Oceanography and Marine Biology: An Annual Review

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OCEANOGRAPHY and MARINE BIOLOGY AN ANNUAL REVIEW Volume 44

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OCEANOGRAPHY and MARINE BIOLOGY AN ANNUAL REVIEW Volume 44 Editors R.N. Gibson

Scottish Association for Marine Science The Dunstaffnage Marine Laboratory Oban, Argyll, Scotland [email protected]

R.J.A. Atkinson

University Marine Biology Station Millport University of London Isle of Cumbrae, Scotland [email protected]

J.D.M. Gordon

Scottish Association for Marine Science The Dunstaffnage Marine Laboratory Oban, Argyll, Scotland [email protected]

Founded by Harold Barnes

Boca Raton London New York

CRC is an imprint of the Taylor & Francis Group, an informa business

CRC Press Taylor & Francis Group 6000 Broken Sound Parkway NW, Suite 300 Boca Raton, FL 33487-2742 © 2006 by R.N. Gibson, R.J.A. Atkinson and J.D.M. Gordon CRC Press is an imprint of Taylor & Francis Group, an Informa business No claim to original U.S. Government works Printed in the United States of America on acid-free paper 10 9 8 7 6 5 4 3 2 1 International Standard Book Number-10: 0-8493-7044-2 (Hardcover) International Standard Book Number-13: 978-0-8493-7044-1 (Hardcover) International Standard Serial Number: 0078-3218 This book contains information obtained from authentic and highly regarded sources. Reprinted material is quoted with permission, and sources are indicated. A wide variety of references are listed. Reasonable efforts have been made to publish reliable data and information, but the author and the publisher cannot assume responsibility for the validity of all materials or for the consequences of their use. No part of this book may be reprinted, reproduced, transmitted, or utilized in any form by any electronic, mechanical, or other means, now known or hereafter invented, including photocopying, microfilming, and recording, or in any information storage or retrieval system, without written permission from the publishers. For permission to photocopy or use material electronically from this work, please access www.copyright.com (http:// www.copyright.com/) or contact the Copyright Clearance Center, Inc. (CCC) 222 Rosewood Drive, Danvers, MA 01923, 978-750-8400. CCC is a not-for-profit organization that provides licenses and registration for a variety of users. For organizations that have been granted a photocopy license by the CCC, a separate system of payment has been arranged. Trademark Notice: Product or corporate names may be trademarks or registered trademarks, and are used only for identification and explanation without intent to infringe. Visit the Taylor & Francis Web site at http://www.taylorandfrancis.com and the CRC Press Web site at http://www.crcpress.com

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Contents Preface

vii

Correction to Volume 43

ix

Review of three-dimensional ecological modelling related to the North Sea shelf system. Part II: model validation and data needs

1

Günther Radach & Andreas Moll

Role, routes and effects of manganese in crustaceans

61

Susanne P. Baden & Susanne P. Eriksson

Macrofaunal burrowing: the medium is the message

85

Kelly M. Dorgan, Peter A. Jumars, Bruce D. Johnson & Bernard P. Boudreau

Mediterranean coralligenous assemblages: a synthesis of present knowledge

123

Enric Ballesteros

Defensive glandular structures in opisthobranch molluscs — from histology to ecology

197

Heike Wägele, Manuel Ballesteros & Conxita Avila

Taxonomy, ecology and behaviour of the cirrate octopods

277

Martin A. Collins & Roger Villanueva

The ecology of rafting in the marine environment. III. Biogeographical and evolutionary consequences

323

Martin Thiel & Pilar A. Haye

Potential effects of climate change on marine mammals

431

J.A. Learmonth, C.D. MacLeod, M.B. Santos, G.J. Pierce, H.Q.P. Crick & R.A. Robinson

Author Index

465

Systematic Index

497

Subject Index

515

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Preface The forty-fourth volume of this series contains eight reviews written by an international array of authors that, as usual, range widely in subject and taxonomic and geographic coverage. The editors welcome suggestions from potential authors for topics they consider could form the basis of future appropriate contributions. Because an annual publication schedule necessarily places constraints on the timetable for submission, evaluation and acceptance of manuscripts, potential contributors are advised to contact the editors at an early stage of preparation. Contact details are listed on the title page of this volume. The editors gratefully acknowledge the willingness and speed with which authors complied with the editors’ suggestions, requests and questions, and the efficiency of Taylor & Francis in ensuring the timely appearance of this volume.

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Correction to Volume 43 Carney, R.S. 2005. Zonation of deep biota on continental margins. Oceanography and Marine Biology: An Annual Review 43, 211–278.

In reviewing various ideas put forward to explain deep benthic depth zonation (Carney 2005), the TROX, Trophic-Oxygen, model for foraminiferan distributions received special mention. This conceptual model incorporates in an easily understood manner several lines of thought concerning the importance of oxygen and labile carbon influx in controlling surficial and interstitial microhabitats. The origin of the TROX model, however, is misattributed to Loubere and his associates (page 228). The TROX model was proposed in the context of microhabitats with Adriatic transect data used as an example by Jorissen et al. (1995). An important feature of the TROX model is the explicit link between oxygen and carbon flux, such that the ecological importance of food availability changes with oxygen concentration. Given adequate oxygen, food is the primary factor. When microbial consumption of higher food levels reduces microhabitat oxygen, then low oxygen can become the primary factor. There have been other attempts to create general foraminiferan distribution models that incorporate both oxygen and carbon flux somewhat similar to TROX. An algebraically formal model of gradient distribution employing the concept of ‘r’ and ‘K’ selected species was developed by Sjoerdsma & van der Zwaan (1992) and tested with mixed success on archived distribution data from the Gulf of Mexico. Unfortunately, the geochemical relationship between oxygen and carbon flux was omitted. Bottom oxygen was estimated from water column profiles, and flux estimated only on the basis of depth. The conceptual model proposed by Loubere et al. (1993) was an assemblage model incorporating both production and taphonomy. Like the TROX model, it is an important contribution to the understanding of trophic control of geographic distribution. That mode links the geochemistry of oxygen and carbon flux. Flux was estimated from sedimentary oxygen consumption; samples were analysed from the western Gulf of Mexico.

REFERENCES Carney, R.S. 2005. Zonation of deep biota on continental margins. Oceanography and Marine Biology: An Annual Review 43, 211–278. Jorissen, F.J., de Stigter, H.C. & Widmark, J.G.V. 1995. A conceptual model explaining benthic foraminiferal microhabitats. Marine Micropaleontology 26, 3–15. Loubere, P., Gary, A. & Lagoe, M. 1993. Generation of the benthic foraminiferal assemblage — theory and preliminary data. Marine Micropaleontology 20, 165–181. Sjoerdsma, P.G. & van der Zwaan, G.J. 1992. Simulating the effect of changing organic flux and oxygen content on the distribution of benthic Foraminifera. Marine Micropaleontology 19, 103–150.

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OCEANOGRAPHY and MARINE BIOLOGY AN ANNUAL REVIEW Volume 44

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Oceanography and Marine Biology: An Annual Review, 2006, 44, 1-60 © R. N. Gibson, R. J. A. Atkinson, and J. D. M. Gordon, Editors Taylor & Francis

REVIEW OF THREE-DIMENSIONAL ECOLOGICAL MODELLING RELATED TO THE NORTH SEA SHELF SYSTEM. PART II: MODEL VALIDATION AND DATA NEEDS GÜNTHER RADACH & ANDREAS MOLL Institut für Meereskunde (IfM), Universität Hamburg (ZMK-ZMAW), Bundesstr. 53, D-20146 Hamburg, Germany E-mail: [email protected], [email protected]

Abstract The aim of this review is to provide an overview of the status of validation of eleven biogeochemical and ecological models of the greater North Sea (COHERENS, CSM-NZB, DCMNZB, DYMONNS, ECOHAM, ELISE, ERSEM, FYFY, GHER, NORWECOM, POLCOMSERSEM) showing the realism achieved as well as the problems hindering a better degree of validity of the models. Several of the models were able to reproduce observations of the state variables correctly within an order of magnitude, but all models are not capable of reproducing every simulated state variable in the range of observations. None of the models can be called a valid model. Comparison of results from different models with datasets are evaluated according to the different spatial and temporal scales, for which data products were available, namely for regional distributions, annual cycles, long-term developments and events. The higher the trophic level, the greater was the discrepancy with the data. Problems still exist in determining the necessary complexity of the ecosystem model. More complexity in the model does not necessarily improve the simulations. Special attention should be devoted to the regeneration mechanisms in the sediments. Species’ groups have been simulated so far with rather limited success. The ecological model simulations did not reproduce fully the observed variability. Possible sources of lacking coincidence with observations originating from the spatial and temporal resolution of the internal dynamics, the trophic resolution, or the resolution of the forcing functions are discussed. Most of the models still need to be evaluated more intensively for their predictive potential to be judged. They have not yet been tested to a degree which is possible today using the various existing datasets from the northwest European shelf seas (presented in the Appendix). Common datasets for the necessary annual cycles of forcing functions are needed.

Introduction The overall aim of this review is to give an overview on the state-of-the-art biogeochemical and ecological three-dimensional modelling related to the marine ecosystem of the greater North Sea. The goal is to provide guidelines for the further development of marine ecosystem models which will be used in the future for making predictions about how the marine ecosystem of the North Sea functions and how concentrations and fluxes of biologically important elements like carbon, nitrogen, phosphorus, silicon and oxygen vary in space and time, throughout the shelf over a timescale of years, in response to physical forcing. Three-dimensional physical oceanographic modelling, which forms the basis of the ecological models, was recently reviewed by Jones (2002). 1

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With respect to future environmental problems occurring in the North Sea, a decadal frame has to be envisaged for modelling. Models are the only tools which can be used as a means to investigate developments of annual cycles and interannual variability in shelf sea systems to be expected in future decades, by simulating scenarios with different initial settings and boundary conditions. This review consists of two parts. Part I (Moll & Radach 2003) described the existing ecological models dealing with the greater North Sea; it characterised the complexity and the achievements of eleven ecosystem models for the whole North Sea or parts of it. Seven of these models are threedimensional models (NORWECOM, GHER, ECOHAM, ERSEM, ELISE, COHERENS, POLCOMS-ERSEM) designed for describing the ecosystem dynamics of the North Sea, based on the physical oceanographic circulation, in more or less detail. Several of the models were used for specific applications, some of which have already been described in the literature. The information about these models and their applications from all available papers were aggregated under the heading of the names of the eleven ecological models in Moll & Radach (2003; their Table 1). This Part II provides an overview of the status of validating these models of the greater North Sea area. The term ‘status of validation’ denotes the current state of realism which a model has reached, as shown by the process of validating the model results by appropriate methods. The status of validation is considered to be a very important property of these models, because it is of great importance for simulating future scenarios that the simulations can realistically reproduce a series of observed annual cycles and especially their observed variability. The aim of this part is not only to show the realism achieved, but also to find out the problems hindering a better degree of validity of the models. The basis for both parts is the published literature on biogeochemical and ecological threedimensional modelling related to the marine ecosystem of the greater North Sea. Although this review is concentrated on the North Sea, the problems arising in modelling other shelf seas and also the oceans in temperate climatic regions are very similar, as the corresponding literature shows. The quality of the simulations is reported on the basis of judgements of the facts given in the publication, in so far as they help to elucidate the achievements and failures of the models. Being restricted to the knowledge contained in the publications, very often questions about causes of failures must remain open. The order of the paper is as follows: after a short recapitulation of the published attempts at validating the models, the applied validation methods and the quantitative measures of the goodness of fit used for evaluating the comparison of simulations and data are briefly reported. Then the validational status of the selected models is discussed in detail with respect to defined space and timescales: The simulation results presented in the available literature are analysed with respect to regional horizontal distributions, to annual cycles and long-term developments, and also the temporal event scale. The discussion brings out common features of success and failure of the models and suggests measures to overcome the problems. A few important datasets available for testing the models are located and briefly described in the Appendix.

Validational efforts for ecological models for the North Sea Before presenting the validational state of the marine ecological North Sea models listed in Table 1, those publications which contain information on validational efforts are summarised. For most of the models their results were compared more or less thoroughly to observations. In a few cases comparisons to common datasets were performed. Nearly all models presented time-series of simulated state variables vs. observed data in graphical form and they presented annual cycles of various state variables in comparison to either observed time-series at special locations or aggregated and averaged box data. While older simulations concentrated on the mean situation, newer papers also compared their simulations with data from actual years. 2

Model name

NORWECOM

GHER

ECOHAM

ERSEM

ELISE

COHERENS

POLCOMS-ERSEM

MIRO

CSM-NZB, DCM-NZB

FYFY DYMONNS

No

1

2

3

4

5

6

7

8

9

10 11

Time-series and averaged box data Mean situation and actual years Graphically, cost function (see Soiland and Skogen, 2000) Averaged box data Mean situation Graphically Averaged box data Mean situation Graphically, cost function (see Moll, 2000) Time-series and averaged box data Mean situation and actual years Graphically, statistical analysis (Pätsch and Radach, 1997) Averaged box data Actual year Graphically Time-series Actual year Graphically Averaged box data Not mentioned Graphically Averaged box data Mean situation Graphically Time-series of station data Mean situation Graphically No validation exercise Averaged box data Actual year Graphically

Characteristic of validational effort: 1. Type of data 2. Actuality 3. Type of validation (if quantitative with citation)

Table 1 Validational efforts for eleven North Sea models

3 1988–1989 1989

1985 1987

1995

1985 1988–1989 1955–1993

1985 1986

1985 1988 1993

Simulation year

None NERC NSP data

Dutch coastal transect data

PHAEOCYC reference station

NERC NSP data ICES data

ECOMOD data, ICES data, Literature data NERC NSP data, NOWESP Time-series data Cruise data, E1 station data French Monitoring Network NERC NSP data

SKAGEX data NERC NSP data ICES data Literature data (NPP only)

Datasets

None Whole area mean Whole time

Parts only Whole time

Whole region Parts only

Unknown Unknown

Not mentioned Whole time

Parts only Whole time

Whole region Whole time

Whole region Parts only

Parts only Whole time

Whole region Parts only

Comparison: 1. In space 2. In time

No (OSPAR et al., 1998)

(OSPAR et al., 1998)

(OSPAR et al., 1998)

No

No

(OSPAR et al., 1998)

(OSPAR et al., 1998), (Skogen and Moll, 2000, 2005) (OSPAR et al., 1998)

(OSPAR et al., 1998), (Skogen and Moll, 2000, 2005) No

References for quantitative model comparison study

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GÜNTHER RADACH & ANDREAS MOLL

The NORWECOM model went through consecutive validational steps. Firstly annual net primary production values were presented as tables (Skogen et al. 1995). Later a comparison of station data from the Norwegian section in the Skagerrak for nitrate and chlorophyll were displayed graphically (Skogen et al. 1998). A comparison of the horizontal distribution for long-term seasonal averages was presented by Soiland & Skogen (2000) showing the observed and modelled distributions, their differences, and the cost function fields for the state variables inorganic nitrogen, phosphate, silicate and chlorophyll for the surface (0–20 m) and for oxygen below 20 m for the whole North Sea. The validational process was continued by comparing data from the TorungenHirtshals section in the Skagerrak area for the years 2000 and 2001 with results from the model (Skogen et al. 2002, 2003). For the ECOHAM model the state variables phosphate and chlorophyll were compared with observed regional long-term monthly means to resolve the annual cycles (Moll 1998). Cost function values were calculated for North Sea wide chlorophyll and phosphate distributions (Moll 2000), and an evaluation of the monthly annual cycles was made for selected boxes. The seasonal dynamics of the North Sea sediments were also simulated by coupling ECOHAM to a sediment model. The evaluation of the validity of the seasonal dynamics in the water column was continued using this extended version of the model (Luff & Moll 2004), including the sediment dynamics, and also validational efforts for the state variables in the sediment were presented. ECOHAM was supplemented by the nitrogen cycle for simulating the annual dynamics; this version was than applied to the Bohai Sea, China (Zhao et al. 2002, Wei et al. 2003). A validation exercise for dissolved inorganic nitrogen concentrations was also performed by Wei et al. (2004), comparing the simulation results with observations from 1998–1999. The model was extended by adding the full carbon cycle (Moll et al. 2003) and this new version (ECOHAM2) was compared to the previous version (ECOHAM1) to illustrate improvements for chlorophyll cycles in winter conditions in the North Sea. It is intended to run ECOHAM2 to study the zooplankton population dynamics of the single species Pseudocalanus elongatus of the North Sea with its physical and biological interactions (Andreas Moll, personal communication 2006). Several papers contributed to an intensive validational effort for the ERSEM model. Comparisons with data exist for all macro-nutrients, silicate, phosphate, nitrate and ammonium (Baretta et al. 1995, Radach & Lenhart 1995) for almost all regions of the North Sea. A detailed comparison of annual cycles for phytoplankton groups was given by Ebenhöh et al. (1997), discriminating diatoms, flagellates and total chlorophyll. Baretta-Bekker et al. (1995, 1997) provided a comparison with data for bacteria, heterotrophic flagellates and microzooplankton annual cycles showing the improvements in process parameterisations from ERSEM-I to ERSEM-II for different coastal boxes. The diagenetic module in ERSEM simulated the nutrient regeneration in the sediments, and Ruardij & van Raaphorst (1995) compared oxygen penetration depth and nutrient profiles for the upper 10 cm for February and August. Observed benthic macrofauna was subject to a comparison by Blackford (1997). In addition to the comparison of the annual cycles of nutrients and phytoplankton with climatological data, Pätsch & Radach (1997) compared corresponding long-term time-series from Helgoland Reede from 1962–1993, including statistical analysis of the observed and simulated variability. ERSEM was applied to the Humber plume area (Allen 1997) with an additional validational step for the annual cycles of nutrients and plankton groups. A validation exercise for oxygen concentrations, chlorophyll and all four nutrients was also performed by Allen et al. (1998), using the results from a water column version of ERSEM for the different regime of the Adriatic Sea. ERSEM is the best studied model. The validational tests of the POLCOMS-ERSEM model presented by Allen et al. (2001) at two sites of the NERC NSP stations used the ERSEM project data for several state variables of nutrients, chlorophyll and plankton groups. This was updated by Allen et al. (2004) studying turbulence as a control parameter in a one-dimensional ERSEM setup coupled to the General Ocean Turbulence 4

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Model (GOTM) (Burchard et al. 1999). The POLCOMS-ERSEM model was used by Proctor et al. (2003) to simulate the seasonal cycle of nutrients (nitrate, ammonium, phosphate and silicate) and primary and secondary production for the year 1995. Also nutrient budgets were calculated and compared with previous estimates. It is intended to run POLCOMS-ERSEM for the full northwest shelf in operational mode on a supercomputer to study eutrophication of the southern North Sea on a 6 km grid (Martin Holt, personal communication 2005). Concerning the ELISE model for the English Channel region simulation results for nitrate, silicate and phytoplankton nitrogen content were compared with data on the basis of an annual cycle for distinct regions of the Channel (Menesguen & Hoch 1997). Long-term simulations were investigated for the Bay of Seine (Guillaud & Menesguen 1998, Guillaud et al. 2000). They provided a validational effort for particulate phosphorus in the sediment. For the one-dimensional version of the COHERENS model Tett & Walne (1995) attempted a validation for three NERC NSP stations over the annual cycle. Lee et al. (2002) reduced the spatial dimensions of the COHERENS model to extend and improve the benthic and pelagic biology in a one-dimensional depth-resolving version of the model (called PROWQM) by coupling the physical and microbiological processes in the water column with the sedimentation, resuspension and benthic mineralisation processes. The results were extensively compared with data and results from studies on models. The three-dimensional model results have not yet been tested against data, but several verification studies were conducted (Luyten et al. 1999). Currently a new physical-biological coupled ecosystem model called ECOSMO for the North Sea and the Baltic Sea is under development (Corinna Schrum, personal communication 2005) using the HAMSOM circulation model (Schrum & Backhaus 1999). The other two-dimensional ecological model systems (CSM/DCM-NZB, MIRO and DYMONNS), which were discussed in Moll & Radach (2003), will also be dealt with because they contributed to North Sea model validation exercises. The DCM-NZB model compared annual nutrient and chlorophyll data for the Noordwijk section and oxygen data for the Terschelling section off the Dutch coast (Peeters et al. 1995). Los & Bokhorst (1997) provided a long-term simulation for reproducing the data from the Noordwijk transect over 20 years, comparing also the mean annual cycles for all nutrients and chlorophyll. De Vries et al. (1998) extended the analysis of the coastal gradients. For the CSM-NZB model a calibration study investigated the whole North Sea simulation in comparison to observed nutrients and chlorophyll (Bokhorst & Los 1997, MARE et al. 2001). A synthesis of the validational exercises on the MIRO model was presented by Lancelot et al. (1997), where observed and predicted nutrients and phytoplankton in terms of chlorophyll and Phaeocystis cells were compared in the Dutch, Belgian and French coastal zones. Lancelot et al. (2005) gave a full representation of the 0-d MIRO model (including the equations), which was set up as a quasi-closed 3-box system. They compared annual cycles simulated under climatological forcing (1989–1999) with data from 1989–2000. The MIRO model (Lancelot et al. 2005) is currently being included into a three-dimensional coupled physical-biological model (MIRO&CO-3D) using the COHERENS physical model (Geneviève Lacroix, personal communication 2005) where simulated chlorophyll is compared with ocean colour data for the year 2003. For the DYMONNS model the total pelagic dissolved nitrogen content was compared against NERC data for the southern North Sea (Kelly-Gerreyn et al. 1997). Hydes et al. (1997) compared monthly primary production values for aggregated ICES boxes. For the FYFY and GHER models there has so far been less effort to validate the models. Seven models of the North Sea ecosystem (CSM-NZB/DCM-NZB, DYMONNS, ECOHAM, ELISE, ERSEM, MIRO, NORWECOM) were compared against common datasets of observations. This model comparison study was conducted by the OSPAR Commission, in a workshop on eutrophication issues, to evaluate the agreement between the results from the models and available observations (OSPAR et al. 1998). The comparison used ‘cost functions’ as defined below in the 5

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section ‘Applied validation methods: Measuring the goodness of the simulations’. This model comparison exercise became a reference for further comparisons which have been mentioned already in the foregoing paragraphs and which will be reported on in the course of this review. Three aspects were investigated: (1) regional distributions, (2) annual cycles and (3) long-term developments. In fact, the available datasets dictated which comparisons between results from the model and data could be made. The following specific datasets, created by averaging observations on different spatial and temporal scales, could be used for such a comparison using cost functions: 1. The dataset for regional distributions resulted from long-term seasonal averaging (e.g., for ‘winter’, averaging data from January and February) of all available data for the whole of the North Sea on a grid of 1˚ longitude and 0.5˚ latitude. 2. The dataset for annual cycles consisted of monthly mean data derived by climatological averaging (over about three decades) for 1˚ longitude × 1˚ latitude boxes for the whole North Sea. 3. The dataset for long-term developments used time-series for up to four decades at specific stations with relatively fine temporal resolution. These and similar datasets (see Appendix) were used in many of the comparisons between simulation results and data products, during the workshop and in later work. In summary detailed quantitative validational efforts were presented for only a few models, like NORWECOM, ECOHAM1 and ERSEM, when applied to some specific regions. These efforts used either the evaluation of a cost function as in OSPAR et al. (1998) or provided a quantitative statistical analysis of observed and simulated variability. Validational exercises were restricted by the available databases. The comparisons may build on averaged box data as climatological means, at best, when aiming at covering the whole North Sea region. However, annual cycles are resolved only by a few datasets, some of which are identified in the Appendix. Observations resolving actual years, like the NERC North Sea Project dataset (see Howarth et al. 1994) are rare. The validational efforts for ERSEM, ECOHAM and NORWECOM were the most intensive. Comparisons of datasets with the results of long-term simulations covering four decades are rarely presented, although observations at Helgoland and other stations (see Visser et al. 1996) exist. Up-to-date observations are, however, rarely obtained directly for model validation purposes.

Validational status of the ecological models for the North Sea Validation of a computational model is the process of formulating and substantiating explicit claims about the applicability and accuracy of computational results, with reference to the intended purposes of the model as well as to the natural system it represents (Lynch & Davies 1995). In this process the results provided by the simulations are tested against the available observations. The logic is as follows: The simulation model is used for reproducing a past situation (which is often called a ‘prediction’; a better term would be ‘hindcast’). The available observations for this past period of time serve as a means to judge the reliability of the simulation. The goodness of the agreement between model results and observations provides the degree of faith in the use of the simulation model for the future, for which, of course, no test against observations can be made beforehand. In a more general understanding of the whole validational process code verification and comparison of observations vs. simulated results are only two aspects of validation, according to Dee (1995). The term ‘conceptual validation’ concerns the formulation of the reduced system of equations. The objective of ‘algorithmic validation’ is to ensure that the finite set of equations was

6

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transformed into a valid finite-dimensional representation. ‘Software validation’ includes all activities which increase confidence in the correctness of the coding. This step is often called ‘model verification’. Finally, the procedure of testing the validity of claims about the functionality of the computational model is called ‘functional validation’, in which it is shown whether or not a model is able to reproduce certain behaviour of the system modelled. The last step is often called ‘model validation’. For further discussion of a proper use of the terms ‘verification’ and ‘validation’ see Popper (1982) and Oreskes et al. (1994). In marine ecological modelling, the term ‘model validation’ is mostly used in the sense as defined above, and the term validation is associated with ‘establishing the agreement between predictions and observations’, as opposed to ‘model verification’, which tends to be used in the sense of ‘checking that the mathematical equations are being solved numerically correctly’. Software validation and functional validation are the only two steps of the several validational steps mentioned which will be discussed in the following sections in some detail. In the reviewed literature the term ‘validation’ has often been used ambiguously. Not only the process of validation (i.e., a ‘validational effort’) was called ‘validation’, but often the authors meant that the procedure in itself ensures the proof that the model is valid: The models were called ‘validated’ when the authors merely performed comparisons between simulation and observations. This rather euphemistic use of the word ‘validation’ is misleading and will not be adopted by us. Performing validational tests does not mean automatically that the tests are successful and the model is valid. The term ‘validated model’ is used for a ‘valid model’, which is a well-tested model that has proven to be realistic and which can be used with confidence in other cases where similar conditions apply (see Popper 1982). In the evaluation a strict differentiation will be made between the ‘effort of validating’ (= process of validation) a model and a possible resulting ‘valid’ model (= positive result of the process).

Model verification status Verification is done for most of the ecological North Sea models by budget calculations. The conservation of mass is taken as evidence that numerics and coding are correct. Budgets were mostly set up for nutrients, for example for total nitrogen or phosphorus in the three phases of dissolved inorganic matter (DIM), dissolved organic matter (DOM) and particulate organic matter (POM). In nearly all the recent papers on modelling statements were included that conservation of mass was achieved. Conservation of mass is only one possible test for correct numerics and coding. The reproduction of simple analytical solutions of the model equations and of laboratory experiments could provide further test cases. A specific additional verification step would be to simulate special solutions of the equations under defined forcing conditions, as is common in marine hydrodynamics. This has been done for hydrodynamic circulation models (Proctor et al. 1997, Delhez et al. 2004) and for turbulence closure models of stratified water columns (Kraus 1977, Baumert & Radach 1992, Burchard et al. 1998, Burchard & Petersen 1999, Jones 2002). There have apparently been no such attempts for the ecological models of the North Sea. It would be desirable for test cases to be developed and that specific scenarios from previous validational initiatives, as for example on eutrophication studies (OSPAR et al. 1998) or on contaminant transport (OSPAR 1998), be repeated.

Applied validation methods: measuring the goodness of the simulations In this section validation methods used for the comparison of the results of simulations of the North Sea models with observations will be presented.

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Methods of validation used for the results from ecological North Sea models are ranked from qualitative/subjective to quantitative/objective and examples are given of their appearance in the literature. Mostly measures of goodness of fit were used which show the agreement of observations and simulations at a special time instant or for an interval at a certain station or for a box by direct comparison. Statistical measures for the whole region and the whole time interval, for which the simulations were performed, are not yet common. Generally speaking, direct comparisons are used when available data are sparse, and statistical measures demand the existence of datasets which are complex in space and/or time. The most common validation procedure consists in comparing data for observed and simulated parameters directly by visual inspection; this method continues to be the standard method used in most of the papers given in Table 1. The types of the graphical representations may vary. Graphical model validation procedures promote, however, a rather subjective evaluation of the goodness of fit when showing, for example, a continuous line for the simulation and crosses for observations. This method was applied to all timescales from the simulation of time-series on the event scale of some days to weeks as, for example, Kühn & Radach (1997; their Figures 4 and 7–10), to simulations of the full annual cycle first published by Horwood (1982; his Figure 10), as well as to long-term simulations by Los & Bokhorst (1996; their Figure 5), and by Pätsch & Radach (1997; their Figures 10 and 11). For stratified areas a separation into surface and bottom layers was necessary to take account of the differences in the model performance in different depth regimes (Figure 5 in Agoumi et al. 1985). In only a few papers comparisons of vertical profiles for different seasons or regions were shown (Figures 12–14 in Gregg & Walsh 1992). For comparisons of the evolution of vertical profiles over the annual cycle, contour plots were provided especially at Ocean Weather Ship positions or at coastal stations with seasonal stratification. This kind of representation is still very common in one-dimensional modelling and was continuously applied to as many state variables as available, for example by Radach (1983; his Figure 8) and by Fasham et al. (1993; their Figure 8). A common method for comparing sparse observational data with the simulation is still to show a table with measured values of process rates found in different references compared to simulated values, for example for cumulated process rates like annual net primary production, sometimes accompanied by illustrations (Figure 11 with table in Moll 1998). The visual comparison of observed and simulated horizontal distributions (Figures 3 and 4 in Pätsch & Radach 1997) and of satellite-derived horizontal features with simulations (Plate 3 in Gregg & Walsh 1992) is common. Three-dimensional simulation models have to use observations which originated from many cruises. The data were usually aggregated into time and space intervals and then averaged, adding statistical information on the standard deviation and the extreme values. Vertical bars indicate monthly means and extreme values of the observations for the annual cycle of different regions (Figures 3 and 5–7 in Fransz & Verhagen 1985). When comprehensive datasets became available, this method became more and more common (Figures 4–8 in Baretta et al. 1995). Only rarely Box-Whisker plots or similar statistics were used for describing the performance of the model vs. the observations, although there should not be any problem using this method as a standard tool in validation exercises. Several statistical methods are available for measuring the goodness of fit, such as covariance analysis, regression analysis, mean square errors or cost functions. All of them are, however, based on the existence of corresponding datasets. Early attempts of validating complex models made use of methods applied in economics (Radford 1979, Baretta & Ruardij 1987). Radford (1979) made use of control charts to find extreme deviations between simulated and observed concentrations; the method of control charts was derived from manufacture control and assumed that successive deviations were statistically independent (Radford & West 1986), which may not be fulfilled for ecological simulations. The BOEDE model was evaluated by Baretta & Ruardij (1987) using the method by Stroo (1986), who defined an overall measure by using the mean square prediction error, normalised by the sum of squares of 8

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predicted values; he then transformed this measure into a function ranging in value between 0 (no agreement) and 1 (perfect agreement). Only a few papers used statistical methods such as regression analysis. Sometimes the temporal means and standard deviations of observed data and simulated data were compared and complemented by correlation coefficients and root mean square errors, for example by Ishizaka (1990), to quantify the deviation between log-transformed observations and simulated concentrations. The ‘cost function’ is a mathematical function which provides a useful means of comparing data from two different sources, for example model results and observations. The cost function gives a nondimensional number which is indicative of the ‘goodness of fit’ between the two sets of data. Sometimes the measure is based on the sum of the absolute differences, sometimes on the squares of the differences. For comparing different models of the North Sea, as presented by OSPAR et al. (1998), the definition of a cost function was based on temporal and spatial means, calculated from both observations and results from the model in the same manner. The cost function was defined as the sum of the absolute deviations of the model values from the observations, normalised by the standard deviations of the observations in each spatial unit (box) and temporal interval (season); thus it is a standardised, relative mean error. According to this scheme two cost functions, regional and seasonal, were applied. The normalised deviation between model result and observation for each box (x) and each season (t) (or more generally: time intervals (t)), Cx,t , was calculated as Cx ,t =

M x ,t − Dx ,t , sd x ,t

(1)

where Mx,t is the mean value of the model results within box x and season t, Dx,t is the mean value of the in situ data within box x and season t, and sdx,t is the standard deviation of the in situ data within box x and season t. The values Cx,t constitute a ‘cost function field (cff)’ when many locations x are given for one time t or a ‘cost function time-series (cfts)’ when many times t are given at one location x. Then the seasonal cost function Ct for the overall mean of all boxes for one season was defined as follows: n

Ct =

∑C

x ,t

x =1

,

n

(2)

where Cx,t is the normalised deviation between model and data for box x and season t, and Ct is the normalised deviation for season t, averaged over all n boxes, where data are available. The regional cost function Cx for the overall mean for all seasons for one box was defined as follows: m

Cx =

∑C t =1

m

x ,t

,

(3)

where Cx,t is the normalised deviation between model and data for each box x per each time interval t (e.g., month), and Cx is the normalised deviation per box, averaged over time, with m being the number of time intervals t, for which observations are available. Many of the ecological North Sea models described above in the section ‘Validational efforts for ecological models for the North Sea’ were used in a comparison using these cost functions 9

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GÜNTHER RADACH & ANDREAS MOLL

(OSPAR et al. 1998). Not every model could, however, deliver the same cost function application because of restrictions of model setup and performance. This comparison is a main source for judging the goodness of fit of the models. For the purpose of categorising the results, the following (subjective) interpretation of the values of the ‘cost functions (cf)’ to measure the goodness of fit between model and data will be used: Rating

Condition

Very good Good Reasonable Poor

0 1 2 3

< < <
3) instead of >5. The cost function approach should become a standard method for model validation.

Validational status of the models The evaluation of the validity of the model simulations will be performed according to different spatial and temporal scales. Such an evaluation is possible for four combinations of spatial and temporal scales: 1. For regional distributions (see section ‘Regional distributions’), described by the largescale structure of the distributions of the state variables in the North Sea, resolved by a box structure, on temporal scales of seasons; 2. For annual cycles (see section ‘Annual cycles’) which were derived for a grid of relatively small boxes over the whole of the North Sea, from climatological averaging of available data per month; 3. For long-term developments (see ‘Long-term developments at specific stations’), for temporal scales up to decades at specific stations with relatively fine temporal resolution; 4. For events (see section ‘Events’) that use special datasets for special model applications. Regional distributions For validating regional distributions of phytoplankton parameters and nutrients, datasets of climatological seasonal or monthly means are available which are based on the order of 105–106 observations per parameter for the whole of the North Sea. One such dataset was provided by the International Council for the Exploration of the Sea (ICES), consisting of long-term averaged, but spatially finely resolved seasonal data (OSPAR et al. 1998); for details see Appendix under ‘ICES dataset’. The validation procedure was performed on five of the twelve models of Table 1 using the same ICES data: CSM-NZB (de Vries et al. 1998), DYMONNS (Hydes et al. 1997), ECOHAM1 (Moll 2000), ERSEM (Pätsch & Radach 1997), NORWECOM2 (Soiland & Skogen 2000). The comparisons were intended to indicate how well the models reproduced the spatial distributions and their gradients in comparison to climatological seasonal average distributions. Only four state variables (chlorophyll, phosphate, dissolved inorganic nitrogen (DIN) and silicate) could be compared, because either the models did not deliver other state variables or corresponding data were not available or both. The regional cost function was used for this comparison (see Equation 3); this statistical measure was defined for the entire area for which ICES data exist (see Appendix). The resulting values of the cost functions for chlorophyll and nutrients are given in Table 2. 10

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VALIDATION OF THREE-DIMENSIONAL ECOLOGICAL MODELLING

Table 2 Comparison of regional distributions for phosphorus, nitrogen, silicate and chlorophyll after the first model comparison study (OSPAR et al. 1998) Model

Simulation year(s)

Depth interval

Winter (JF)

Spring (MJJ)

Summer (JAS)

Chlorophyll ERSEM ECOHAM1 NORWECOM ERSEM ECOHAM1 NORWECOM DYMONNS CSM-NZB

1985 1985 1985, 1988, 1993 1985 1985 1985, 1988, 1993 1988–1989 1985

0–20 m 0–20 m 0–20 m 20 m–bottom 20 m–bottom 20 m–bottom Depth averaged Depth averaged

3.98 7.61 2.62 7.61 10.24 5.78 4.72 5.80

5.27 6.05 4.06 3.36 3.12 2.51 4.84 3.70

2.93 2.05 1.25 3.05 2.14 1.68 2.31

Phosphorus ERSEM ECOHAM1 NORWECOM ERSEM ECOHAM1 NORWECOM CSM-NZB

1985 1985 1985, 1988, 1993 1985 1985 1985, 1988, 1993 1985

0–20 m 0–20 m 0–20 m 20 m–bottom 20 m–bottom 20 m–bottom Depth averaged

1.03 1.03 1.38 1.09 1.04 1.59 2.20

1.32 1.51 2.40 1.18 1.99 2.90 3.70

1.69 1.90 3.26 0.90 1.85 2.33

DIN NORWECOM NORWECOM CSM-NZB

1985, 1988, 1993 1985, 1988, 1993 1985

0–20 m 20 m–bottom Depth averaged

2.50 1.83 3.90

11.30 9.51 5.20

23.04 14.26

Silicate NORWECOM NORWECOM CSM-NZB

1985, 1988, 1993 1985, 1988, 1993 1985

0–20 m 20 m–bottom Depth averaged

1.64 1.25 1.40

2.21 2.64 3.40

1.74 1.46

Notes: The second column describes the simulated years, followed by the selected depth ranges for comparison with surface (0–20 m) or bottom (20 m–bottom) observations. The last three columns describe the values of the cost function for three seasons: JF = January/February, MJJ = May/June/July, JAS = July/August/September. For explanation of the cost function see section on “Applied validation methods: Measuring the goodness of the simulations.”

For chlorophyll all models (CSM-NZB, DYMONNS, ECOHAM, ERSEM, NORWECOM) for the greater North Sea were included in the comparison. The goodness of fit in the upper layer was ‘good’ to ‘reasonable’ only for the summer period, and ‘poor’ for autumn and winter, except for NORWECOM in winter. It is remarkable that no model provided a good representation of the regional chlorophyll distribution in spring. One should consider, however, that climatological mean distributions, as represented by the data used, average out the specifics of the actual distributions (e.g., high spring blooms in different weeks of special years). Therefore, this kind of comparison must be valued with caution. The behaviour of the models could probably be much more realistic than can be seen from this comparison. Phosphorus and silicate distributions were the parameters that gave the best simulations. The goodness of fit was for all seasons ‘good’ to ‘reasonable’ for the models ECOHAM, ERSEM and 11

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GÜNTHER RADACH & ANDREAS MOLL

NORWECOM. CSM-NZB provided reasonable winter distributions. Horizontal distributions of inorganic nitrogen (DIN) provided by NORWECOM and CSM-NZB were also compared to the common datasets. The fit was ‘good’ for winter bottom values from NORWECOM, however, the winter distributions in the upper layer were less satisfying for the models CSM-NZB and NORWECOM. For summer and autumn both models failed to reproduce realistic mean seasonal distributions (cf >5). Although ERSEM has the potential to simulate inorganic nitrogen nutrients and silicate, these two parameters were not included in this comparative study. Soiland & Skogen (2000) presented a repetition of the ASMO Workshop comparison (OSPAR et al. 1998) obtained with the updated version 2 of NORWECOM using the ICES dataset (see Appendix). This study provided an extended comparison of the horizontal distributions with mean seasonal long-term averages (again for the period 1980–1989) showing maps of the observed and modelled distributions, their differences and the cost function fields according to Equation 1 for the state variables inorganic nitrogen, phosphate, silicate, chlorophyll and oxygen for the surface (0–20 m) and below 20 m (Figure 1). The low cost function field values within the interval –1 and 1 (except for a few small areas) for predicted temperature and salinity (Figures 2 and 4 in Soiland & Skogen 2000) indicated a proper representation of the climatological mean hydrographic and circulation fields. In contrast to the results published by OSPAR et al. (1998), the surface chlorophyll cost function values (Figure 4, Table 2 in Soiland & Skogen 2000) improved (winter: 1.61, spring: 1.50, summer: 1.17) in comparison to the previous NORWECOM1 version. The chlorophyll and oxygen horizontal distributions of the cost function values exhibited many white areas due to the absence of observations (Figure 1 (B) and (C)). The areas of stronger deviation concentrated on the Dogger Bank region. Also for phosphate the horizontal distributions exhibited large areas between cost function field values of –1 to +1 and (small or large) islands of large cost function field values (Figure 1 (E)). Phosphate had the best cost function field values in the surface layer (winter: 0.90, spring: 1.25, summer: 1.50) and silicate followed (winter: 1.44, spring: 0.76, summer: 1.28). Areas of large deviations for the nutrients phosphate and silicate lay off the U.K. coasts and in the Skagerrak. Inorganic nitrogen failed again except for winter values (cf in winter: 1.74, spring: 9.57, summer: 13.60) and eastern North Sea coastal areas, with large discrepancies in the central and northern part of the North Sea (Figure 1 (D)). NORWECOM simulated most of the state variables with good cost function field values for most of the North Sea, but failed for the state variable inorganic nitrogen. The authors attributed the failure to the missing observations of ammonium which were responsible for the discrepancies in the comparison between the model state variable DIN and the observed nitrate, especially in summer surface layers. On a finer regional scale with a resolution of 4 km, the model NORWECOM was applied to simulate the ecosystem in the Skagerrak (OSPAR et al. 1998). The cost function field was determined using data from Skagerrak sections and 25-hour averaged simulated values, interpolated on the computational grid (OSPAR et al. 1998, p. D-4). At sections F and H (for their exact positions see Skogen et al. 1998; Figure 2) the cost function values were determined (Table 3), yielding values for DIN, DIP and silicate between 1.47 and 6.03; the values for salinity and temperature were between 1.97 and 5.36, indicating, in our view, that there was a problem in correctly meeting the actual physical situation. For the ECOHAM model, Moll (2000) gave a detailed presentation of the complete results provided for the comparison during the ASMO Workshop (OSPAR et al. 1998) and presented the North Sea wide spatial variation of the cost function fields according to Equation 1 for chlorophyll and phosphate in the surface layer for the winter, spring and summer seasons. Climatological mean concentrations provided by the ERSEM II and ICES datasets (see Appendix) were compared with a single year simulation for 1985. Phosphate winter values in January and February (Figure 2) in the upper layer were in best agreement with observation (cf = 1.03), but were also good during 12

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VALIDATION OF THREE-DIMENSIONAL ECOLOGICAL MODELLING

Figure 1 Regional distribution of cost function field values for (A) temperature, (B) surface chlorophyll, (C) oxygen, (D) inorganic nitrogen, (E) phosphate and (F) silicate during May-June-July in the upper 20 m, except for oxygen (20 m–bottom). The isolines of the cost function values are given for the values –3, –2, –1, 0, +1, +2, +3. The simulation was performed with NORWECOM for 1980–1989 and then the results were averaged for the season indicated. (From Soiland & Skogen 2000. With permission from Elsevier.)

13

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GÜNTHER RADACH & ANDREAS MOLL

Table 3 Comparison of phosphorus, nitrogen, silicate, temperature, salinity, inorganic suspended matter and chlorophyll for different regions according to the first model comparison study (OSPAR et al. 1998) a) Regional cost function results for the Belgian-Dutch coast: Location: Terschelling

Noordwijk

Model

State Variable

T10

T50

N10

N50

DYMONNS

Chlorophyll DIN total N Chlorophyll DIN Chlorophyll DIN

0.45 1.12 0.88 0.38 1.02 0.18 0.57

0.64 2.34 1.61 1.01 1.53 0.48 0.86

0.27 1.18 1.01 0.47 0.84 0.66 1.36

1.38 6.36 4.95 0.67 2.05 0.50 1.22

DCM-NZB CSM-NZB

b) Regional cost function results for the Belgian coast: Model

State Variable

MIRO

Chlorophyll Ammonium Nitrate Phosphate Silicate

Belgian CZ 0.32 1.49 0.47 1.04 0.64

c) Regional cost function results for the English Channel:

Model

State Variable

ELISE

Chlorophyll DIN DIP Silicate Temperature

Location 1 03˚53′30″ W 48˚46′50″ N

Location 2 04˚5′30″ W 50˚0′00″ N

Location 3 01˚35′00″ W 48˚41′30″ N

Location 4 00˚07′30″ E 49˚26′00″ N

Location 5 01˚21′30″ E 50˚49′00″ N

0.39

0.98 0.29 0.12 0.27 0.09

0.64 0.57 0.49 0.78 0.09

0.29 0.23 1.38 0.50 0.11

0.87 0.17 0.19 0.31 0.07

d) Regional cost function results for two sections in the Skagerrak:

Model NORWECOM

State Variable Salinity Temperature DIN DIP Silicate

Location Section F

Section H

5.36 4.54 2.15 2.12 4.87

1.97 3.47 6.03 2.97 1.47

spring (cf = 1.51) and summer (cf = 1.90). During summer there was most deviation in the bottom values due to a fast remineralisation at the bottom. Chlorophyll showed good agreement only in the summer (cf = 2.05, Figure 5 in Moll 2000); it was overestimated by the simulation in coastal 14

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VALIDATION OF THREE-DIMENSIONAL ECOLOGICAL MODELLING

61

60

NORWAY

59

SWEDEN

58

57

SCOTLAND

DENMARK 56

55

54

GERMANY THE NETHERLANDS

53

0.00 - 0.50

ENGLAND

WALES

0.50 - 1.00

52

1.00 - 1.50

BELGIUM

1.50 - 2.00

51

2.00 - 2.50 FRANCE

50

2.50 - 3.00 > 3.00

Institute für Meereskund Unversitat Hamburg

49 -5

-4

-3

-2

-1

0

1

2

3

4

5

6

7

8

9

10

11

12

13

14

Figure 2 Absolute cost function field values of surface phosphate in January and February simulated by ECOHAM1. (From Moll 2000. With permission from Elsevier.)

areas in winter (cf = 7.61) and in the central North Sea in spring, resulting in high cost function values (cf > 6). The bloom was well simulated in the northern North Sea. The comparison between the variability of primary production estimates for 10 years from both, ECOHAM and NORWECOM (Skogen & Moll 2000, 2005) gave the important results that the variability in primary production was similar for the two models in each of the areas inspected and that the regional variations were larger than the differences between the two models (Figure 3). For the ERSEM model (130-box version) a regional comparison was performed on a decadal timescale. From the long-term simulation Pätsch & Radach (1997) derived a decadal mean of the simulation results for the period 1984–1993 in the same way as for observations for phosphate and nitrate in the upper 30 m. For both parameters the regional distribution of the observations (Figure 4) exhibited a higher level of concentrations, especially in the coastal areas where the rivers Rhine and Elbe enter, degrading toward the central North Sea, where the concentration levels were quite well mapped. This may indicate that either the river inputs were too low or that the conversion of the nutrients in the coastal sea was not adequately modelled. 15

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GÜNTHER RADACH & ANDREAS MOLL

Figure 3 Annual mean production and its standard deviation for each individual ERSEM box, based on simulation runs with the NORWECOM and ECOHAM1 models for the years 1985–1994. (From Skogen & Moll 2005. With permission from Elsevier.)

In five areas of the English Channel the results of a simulation for 1980 with the ELISE model (Hoch & Garreau 1998; Figure 6) were compared to phytoplankton nitrogen observations mainly collected from 1975–1984. The spatial variations were reproduced as observed for the spring bloom period, but seem to be underestimated for the summer period. A comparison of the simulation from the MIRO model (Lancelot et al. 1997; Figures 6 and 7) for the French, Belgian and Dutch coastal zones showed that the observed range of concentrations of chlorophyll and the nutrients (nitrate, phosphate and silicate) between 1988 and 1993 could be reproduced grossly. The strong north-south gradient along the continental coast was well reproduced. Bokhorst & Los compared their simulation using the CSM-NZB model for winter 1985 (Figures 6.1–6.4 in Bokhorst & Los 1997) with the observed horizontal distributions provided by the ERSEM II dataset (see Appendix). The simulation reproduced the coastal to central North Sea gradient for all nutrients (nitrate, phosphate and silicate) in winter. The comparison for chlorophyll in May 1985 illustrated that the model was able to reproduce the high chlorophyll concentrations in the continental coastal strip, but overestimated the typically observed concentrations in the central and northern North Sea (Figure 5). The comparison of the simulation from the DCM-NZB model with long-term mean data from the Dutch monitoring programme covering the years 1975–1995 (de Vries et al. 1998) concentrated on the phosphate, DIN and chlorophyll along the Noordwijk transect off the Netherlands (Figure 6). The overall near-shore gradient (0–70 km) was reproduced well for chlorophyll, DIN and phosphate, except for phosphate and chlorophyll within the first 5 km off the coast, where the concentration of chlorophyll was overestimated and phosphate was underestimated by the simulation. For the GHER model only primary production values were compared (Delhez 1998); the right level of primary production was met in ICES box 4 (Netherlands coast); observations of primary 16

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VALIDATION OF THREE-DIMENSIONAL ECOLOGICAL MODELLING

(A) Hindcast: 1984 – 1993

(B) Observations: 1984 – 1993

(C) Hindcast: 1984 – 1993

(D) Observations: 1894 – 1993

Figure 4 Horizontal distributions in the surface waters (0–30 m) for (A) simulated and (B) observed phosphate and (C) simulated and (D) observed nitrate in winter (December, January, February) as means over the years 1984–1993 (in mmol m–3); the simulated values resulted from the 40-year long simulation with the 130-boxversion of ERSEM. (From Pätsch & Radach 1997. With permission from Elsevier.)

production were underestimated in ICES boxes 1 (northern North Sea), 2b (Shetland Channel inflow area) and 5 (German Bight), and overestimated in ICES boxes 3a (Scottish coast), 3b (English coast), 7a (central North Sea) and 7b (Dogger Bank). 17

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GÜNTHER RADACH & ANDREAS MOLL (A)

(B)

ERSEM130.MAP

NZBLOOM.MAP

>8

>8

>4

>4

>2

>2

>1

>1

>0.5

>0.5

>0.25

>0.25

>0

egg > testes > ovary, midgut gland > muscle > haemolymph. Even when animals are exposed to elevated Mn concentrations, as in environments that are polluted (industrial waste), acidic (lakes and rivers) or hypoxic (mainly eutrophic marine areas), the relative relationship between the exoskeleton, gills, midgut gland, muscle and haemolymph holds, though concentrations are higher than in animals from pristine areas (Table 2).

The routes and effects of manganese In the following sections an up-to-date review on the routes and effects of manganese in crustaceans is presented. In Figure 1 the uptake of manganese from water is described as well as the accumulation and effects in separate target tissues. Existing data on elimination kinetics are described under the respective tissue section.

Uptake of manganese from water For many organisms the key determinant that influences metal accumulation from water is the speciation of the metal. Metals are usually considered more bioavailable as free ions than as complex ligands with anions. In sea water as much as 58% of the total Mn concentration is free hydrated ions whereas 37% is complexed with chloride, 4% with sulphate and 1% with carbonate (Simkiss & Taylor 1989). Hydrated ions are clearly larger than the equivalent ions in a crystal. These hydration properties of ions in aqueous solution are important in determining the permeability and selectivity of ions crossing membranes (Simkiss & Taylor 1989). Of the borderline metals, only Mn has a sufficiently low enthalpy to be able to shed its hydration and pass through membrane channels. The uptake of divalent trace metal ions occurs mainly at permeable respiratory surfaces, for example gills, and is driven by passive diffusion via ligand binding occurring through calcium channels (Rainbow 1997). Gills Crustaceans are relatively impermeable animals, having the main part of the body covered with a calcareous exoskeleton. The uptake of ions, including metals, dissolved in water thus occurs largely 67

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SUSANNE P. BADEN & SUSANNE P. ERIKSSON

Table 2 Manganese concentrations in field-caught crustaceans from pristine, polluted (industrial waste), acidic (lakes and rivers) and hypoxic (eutrophic) areas Habitat/Order/Species Marine Amphipoda Talitrus saltator Thoracica Tetraclita squamosa Decapoda Callinectes sapidus

Portunus pelagicus

Nephrops norvegicus

Freshwater Decapoda Cambarus bartonii

Orconectes virilis

Potamonautes warreni

Tissue

Total

Pristine

31

Total (–shell)

6.7

Gills Midgut gland Muscle Gills

Polluted

Acidic

Hypoxic

105

References

Rainbow et al. 1998

64

Blackmore 1999

56 16 4.0 0.6

83 29 6.6 1.0

Midgut gland

0.1

1.6

Muscle

0.7

1.9

Weinstein et al. 1992 Weinstein et al. 1992 Weinstein et al. 1992 Al-Mohanna & Subrahmanyam 2001 Al-Mohanna & Subrahmanyam 2001 Balkas et al. 1982, Al-Mohanna & Subrahmanyam 2001 Eriksson & Baden 1998 Eriksson & Baden 1998 Eriksson & Baden 1998

Exoskeleton Gills Haemolymph

223 58 3.3

304 1560 4.3

Total Exoskeleton

52 32

68 102

Midgut gland Exoskeleton Gills Muscle Total Exoskeleton Gills Midgut gland Muscle

11 86 23 6.0 239 340 508 374 87

59

662 1203 886 773 168

513 248 337 106 36 4.5

Alikhan et al. 1990 Alikhan et al. 1990, Young & Harvey 1991 Alikhan et al. 1990 Young & Harvey 1991 Young & Harvey 1991 Young & Harvey 1991 Sanders et al. 1998 Steenkamp et al. 1994 Steenkamp et al. 1994 Steenkamp et al. 1994 Steenkamp et al. 1994

Notes: All concentrations are given as mean µg Mn g–1 dry weight tissue, except haemolymph which is in wet weight.

through the gills (Rankin et al. 1982). The diffusion over the gill membrane is dependent on the concentration gradient of free metal ions. Crustaceans may accumulate essential as well as nonessential metals above the concentration of the medium as the metals may bind to e.g., blood proteins and thus maintain an inward flux (Baden & Neil 1998). The mean Mn concentration in animals from pristine areas is 100 µg g–1 dw, but varies from 0.6–508 µg g–1 dw (Table 1). During hypoxia in the SE Kattegat, Sweden, in 1995, the mean gill concentration of Mn in Norway lobster (Nephrops norvegicus) increased by 30 times to 1560 µg Mn g–1 (Eriksson & Baden 1998; Table 2). The fraction of absorbed and adsorbed Mn is poorly investigated. However, in the SE Kattegat, a black layer of precipitated Mn on the gills was observed indicating that large amounts of adsorbed Mn may occur in the field (Baden et al. 1990). The effects of the precipitated layer of Mn on respiration is not yet investigated but it may hamper a normal function and internal hypoxia may 68

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ROLE, ROUTES AND EFFECTS OF MANGANESE IN CRUSTACEANS

Immune Suppression √ No synthesis of Hc in hypoxia √

Mn (ll)

Mn

Mn (ll)

O2 uptake/ respiration?

Gills

Stomach

Antennulae

Haematopoetic tissue

Haemolymph

Nerve tissue

Midgut gland

Reproductive organs

Muscle

Storage √ Necrosis ?

Fertility ?

Reduced muscle function √

Reduced chemosensitivity √

Figure 1 Routes and effects of manganese in a crustacean. Dissolved Mn II in water may enter via the gills or antennules or get precipitated on the exoskeleton. Entrance may also occur via the food in a variety of chemical form. Octagonal boxes indicate the route and target tissues of Mn and square boxes indicate the effects of Mn exposure. Observed effects (√) and hypothetical but not yet investigated effects(?).

develop, as has been found by Spicer & Weber (1991) for crustaceans when exposed to other essential metals like Cu and Zn. Since the gills are part of the exoskeleton, changes in Mn concentration during the moult cycle follow the same pattern in these two tissues (Eriksson, 2000a). This is further discussed in the section ‘Exoskeleton’ below. Haemolymph Having passed the gill epithelium, Mn is transported in the haemolymph to target tissues either dissolved in the plasma or bound to the haemolymph proteins, predominantly (80–90%) to the respiratory protein haemocyanin (Baden & Neil 1998). Exposing N. norvegicus to realistic concentrations of dissolved Mn (5 and 10 mg Mn l–1 for 2 weeks) the haemolymph plasma reaches the same concentration as the ambient water, whereas the Mn concentrations of the haemocyanin and whole haemolymph (plasma and haemocyanin) are about twelve and three times higher, respectively (Baden & Neil 1998). However, when N. norvegicus were exposed to Mn concentrations of 60 mg Mn l–1 for 2 weeks the plasma and whole haemolymph reached only 0.5 and 1.5 times the concentration of the ambient water (Selander 1997). The biological half-life for manganese accumulation in N. norvegicus during exposure to 5 and 10 mg Mn l–1 and elimination in undosed sea water is relatively fast in haemolymph (about 24 h for both processes) (Baden et al. 1999). As the competitive binding of metals by organic ligands (the Irving-Williams series) is stronger for Cu2+ than Mn2+ (Rainbow 1997), Mn does not replace Cu as apostethic metal in the haemocyanin, as indicated by a constant Cu concentration with increasing Mn concentration of the haemolymph (Baden & Neil 1998). Removal and displacement of Ca from haemocyanin may change the quaternary structure and thus the functional properties of the haemocyanin (Van Holde & Brenowitz 1981, Brouwer et al. 1983). The binding of Cd and Zn is stronger than Ca and has been shown to replace Ca in the haemolymph of the blue crab, Callinectes sapidus. Even though Mn binds slightly stronger than Ca, 69

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no change in Ca concentration of whole haemolymph was found in Nephrops norvegicus with increasing exposure to Mn of 60 mg l–1 (Selander 1997). This constancy in the whole haemolymph, however, does not rule out the possibility that Mn has displaced Ca from the haemocyanin to the plasma. An important source of Mn in the ocean is from hydrothermal vents. The crustaceans adapted to live close to these vents may hypothetically contain a higher concentration of Mn than non-vent crustaceans. Professor J.J. Childress from the University of California, Santa Barbara, kindly provided the authors with haemolymph from a vent crab, Bythograea thermydon, which was found to have Mn concentrations between 0.44 and 1.6 µg g–1 ww. These Mn concentrations are within the range of haemolymph concentration from non-vent crustaceans as seen from Table 1. The maximum mean Mn concentrations of 7.35 µg g1 ww in a field-caught crustacean (Nephrops norvegicus) is reported from the SE Kattegat following a hypoxic period in 1995 (Eriksson & Baden 1998). The effects of manganese on haemocyanin synthesis and adaptation to hypoxia are described in a subsequent section discussing the midgut gland, as this is the primary organ for haemocyanin synthesis (Taylor & Antiss 1999). The synthesis of haemocytes takes place in the haematopoietic tissue localised as a thin sheet on the dorsal site of the stomach in crustaceans (Chaga et al. 1995). The haemocytes of crustaceans consist of hyaline, semigranular and granular cells playing an important role in, for example, the innate immune defence (Ratcliffe & Rowley 1979, Söderhäll 1981, Söderhäll & Cerenius 1992). Immunotoxicology of invertebrates is an unexplored field and as a result no early investigations can be cited. Recently, Hernroth et al. (2004) discovered that when exposed to 20 mg l–1 Mn for 10 days several immunological processes of N. norvegicus were affected. The number of haemocytes decreased by 60%. Despite the great loss of haemocytes, renewal through increased proliferation of the haematopoietic stem cells did not appear to occur. Additionally, maturation of the stem cells to immune-active haemocytes was inhibited in Mn-exposed lobsters (N. norvegicus). To release the prophenoloxidase system (ProPO), which is necessary for the immune defence of arthropods, the granular haemocytes must degranulate. This degranulation activity was also significantly suppressed after Mn treatment. Furthermore, the activation of ProPO by the non-self molecule, lipopolysaccaride, was blocked. Probably Mn replaces Ca and thereby inhibits protein required for mobilisation and activation of the haemocytes. Immune suppression may explain the occurrence of shell disease caused by microbial infection of the exoskeleton in blue crab, Callinectes sapidus, from North Carolina, U.S. (Weinstein et al. 1992). The infection is related to elevated Mn concentrations in the body tissues. Similar findings might explain the high frequency of the parasitic dinoflagellate Hematodinium sp. that has been found in Nephrops norvegicus from the west coast of Scotland (Field et al. 1992). In the same area high concentrations of Mn have been recorded in the tissue of this species (Baden & Neil 1998). Midgut gland In contrast to other target tissues, where manganese accumulation reaches an equilibrium determined by the exposure concentration within 5 days, the midgut gland of N. norvegicus continuously accumulates manganese at a relatively slow rate and does not reach equilibrium after a 3-week period of exposure. This slow accumulation to the hepatopancreas has also been observed for zinc in Carcinus maenas by Chan & Rainbow (1993). The elimination rate of manganese from the midgut gland is, however, much faster. The biological half-lives for accumulation and elimination of manganese are about 4 and 1.5 days, respectively (Baden et al. 1999). Insoluble granules containing metals bound with phosphorus or sulphur have been observed in the epithelial cells of the midgut gland (or comparable organ) in many invertebrates (for review see Ahearn et al. 2004). The granules scavenge and detoxify surplus metals, and are later eliminated through exocytosis. Several marine snails have been shown to eliminate manganese this way (Simkiss 1981, Nott & 70

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Nicolaidou 1994). Although no such granules have yet been described in manganese-rich crustaceans, the surplus of manganese is clearly delivered to the midgut gland for net accumulation as indicated in Rainbow (1997) and Baden et al. (1999). Accumulation is also demonstrated by the relatively high levels of Mn in midgut glands from different species of crustaceans (Table 1). The highest mean tissue concentrations found in the literature are from the midgut glands of a marine hermit crab, Clibanarius erythropus (1596 µg Mn g–1 dw) and a freshwater crayfish, Procambarus clarkii (1677 µg Mn g–1 dw), both collected in areas with known anthropogenic input (Gherardi et al. 2002, Nott & Nicolaidou 1994). Unfortunately, no background data are available for either of these species which is why they have not been included in Table 2. However, unpublished data on background Mn concentrations in another marine hermit crab, Pagurus bernhardus, varied from 15–28 µg Mn g–1 dw in the midgut gland (Andersson 1993), and the highest overall midgut gland background concentration published is 374 µg Mn g–1 dw in a freshwater crayfish, Potamonautes warreni (Steenkamp et al. 1994; Table 1). The synthesis of haemocyanin is primarily recognised to take place in the midgut gland (Taylor & Antiss 1999, for review). In a recent study the combined and separate effects of hypoxia (2.5 mg l–1) and manganese (20 mg l–1) on the haemocyanin concentration were investigated after an exposure period of 2 weeks. Crustaceans adapt to hypoxia by increasing or decreasing (depending on the initial value) the haemocyanin concentration, presumingly to an optimal concentration (Spicer & Baden 2001). A simultaneous exposure to manganese affects this adaptation by preventing the synthesis of haemocyanin (Baden et al. 2003). Muscle The manganese concentration of the muscle tissue remains relatively constant throughout the moult cycle and is less dependent on the exposure concentration of Mn compared with other tissues (Bryan & Ward 1965, Baden et al. 1995, Baden & Neil 1998, Eriksson & Baden 1998, Bjerregaard & Depledge 2002). This constancy is especially interesting since the muscle is a metabolically active tissue with high mitochondrial content. Calculations indicate that an increase in Mn concentration of muscle tissue after exposure to elevated Mn concentrations can, in principle, be explained by the increase in Mn in the extracellular haemolymph of the muscle tissue (Hille 1992, Baden et al. 1995). A plausible explanation for the relatively stable concentration in the muscle cells themselves is, thus, either that turnover rates of manganese in these cells are high enough to disguise increased uptake (at least for the exposure concentrations that have so far been studied) or that the metal never enters the muscle cells but remains in the extracellular haemolymph. Normal muscle concentrations of Mn lie in the range of 0.4–8.0 µg Mn g–1 dw with the exception of the extremely high values of 24 µg Mn g–1 found in small Carcinus maenas by Bjerregaard & Depledge (2002) and 87 µg Mn g–1 found in the freshwater crayfish, Potamonautes warreni by Steenkamp et al. (1994). Many values in the literature are stated as wet weight concentrations with the primary objective being risk assessment of heavy metals in human food. Taken that the daily recommended intake for humans is 2.5–5 mg Mn day–1, a person would have to eat ca 1 kg of crustacean meat just to fulfil the daily requirement. Manganese at natural levels in crustaceans is thus not likely to pose a threat for human consumption. When lobsters (Nephrops norvegicus) are exposed to 10 mg Mn g–1 their muscle extension and thus most probably (consequently) the swimming capacity is affected as will be discussed under the section ‘Nervous system’. Exoskeleton Due to its chemical properties, manganese is found in highest concentrations in the calcified parts of crustaceans, mainly in the exoskeleton, gills and the gastric mill of the stomach (Bryan & Ward 71

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1965, Baden et al. 1990, 1995, Eriksson & Baden 1998, Eriksson 2000a). Depending on the thickness of an animal’s exoskeleton the vast majority of manganese is found in this tissue, as it contains more than 98% of the total Mn content of the decapod lobsters Homarus gammarus (Bryan & Ward 1965) and Nephrops norvegicus (Baden et al. 1995). The manganese incorporated in the matrix of the exoskeleton is believed to have little effect on the animals. The manganese concentration of the exoskeleton changes during the moult cycle, and lobsters (N. norvegicus) collected in the field show a step-wise increase in average Mn concentration from postmoult, intermoult to premoult (Eriksson & Baden 1998). The crustacean moult cycle is dominated temporally by the intermoult phase, with brief periods of postmoult and premoult. There is, however, no correlation between the contemporary environmental Mn(II) concentration of ambient sea water and that of the exoskeleton in field-caught intermoult lobsters (Eriksson & Baden 1998). It was thus proposed that the amount of Mn found in the exoskeleton of intermoult individuals primarily depends on the Mn concentration to which the animals are exposed during the calcification process at postmoult, rather than the current ambient Mn concentrations (Eriksson & Baden 1998, Eriksson 2000a). During growth, the shell of the barnacle Balanus amphitrite has been shown to incorporate Mn in direct proportion to the concentration of the sea water (Hockett et al. 1997). Unlike most crustaceans, the calcified shells in barnacles grow more or less continuously (Bourget & Crisp 1975), thus having continuous calcification. In most crustaceans, however, calcification occurs during a short postmoult period. To test the theory, newly moulted Nephrops norvegicus were exposed to flow-through sea water with R or KI > KIc), fracture occurs (Anderson 1995). Cracks propagate in the direction of least resistance. In a homogeneous, isotropic material (e.g., gelatin), a crack will propagate perpendicular to the direction in which the force is exerted. An animal burrowing by crack propagation in an elastic solid such as gelatin theoretically can make the crack turn by applying force at an angle. Heterogeneous materials (e.g., mud) exhibit smallscale variation in material properties, such as KIc and R, which can result in stochastic changes in the direction of crack propagation (Figure 4). Excess energy can be released by crack branching, which in a heterogeneous material could be a mechanism of particle release. When a crack approaches an interface, if the adhesion at the interface is much less than the cohesion of the material, as is generally the case, the crack will follow the interface (Cook & Gordon 1964). The stress field in front of a crack pointed toward a perpendicular interface has tension pulling the material away from the interface toward the crack. This tension can result in separation at the interface before the crack reaches it, so that when the crack tip hits the interface, a crack oriented along the interface has already been formed and crack resistance is low (Figure 5). The crack preferentially follows the interface, and additional energy is required for the crack to branch away. Materials that resist crack propagation have high toughness compared with easily fractured brittle materials (Gordon 1976). Toughening mechanisms include plastic deformation, interfaces, crack bridging, and crack-tip blunting. Crack bridging is common in polymeric materials (like the mucopolymer matrix in muds) and involves fibres extending across the crack that take energy to break before the crack can propagate. Styrofoam provides a classic example of crack tip blunting: a crack in a porous foam reaches a pore and the crack tip radius is significantly increased, reducing the stress amplification factor. When the plastic zone at the crack tip is large, energy is used for plastic deformation in addition to the energy to propagate the crack. Marine muds, similar to polymer gels (because they appear to comprise grains embedded in polymer gels, cf. Watling 1988), are viscoelastic, and viscous flow or creep may be an important toughening mechanism on particular spatial and temporal scales. The behaviour of viscoelastic materials is time-dependent: under high strain rates, the material behaves elastically, whereas under low strain rates, viscous flow occurs. The dimensionless ‘Deborah number (De)’ is defined as the ratio of the time a process takes to the time required for significant plastic deformation to occur (Reiner 1964). Solids have very small values of De, fluids very large. Viscoelastic materials have

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15

A

15

B

20

C

20 25 30 y

30

Crack 25 Tip 25

x

38 35

25 25

D

35 30 25 20 20 15

15

Figure 5 (A) The stress field (σ x) around a crack tip. The stress in the x direction (parallel to the direction of crack propagation) relative to the far-field stress [dimensionless] is shown. Maximal stress a short distance in front of the crack is tensile, so that when the crack approaches a weak interface (B), separation occurs at the interface before the crack reaches it (C). When the crack tip reaches the interface, the crack follows the interface (D). A weak interface is one for which cohesion of the material is much greater than adhesion between the two materials at the interface. In the illustration the dark black lines represent a rigid surface, such as an aquarium wall. (From Cook & Gordon 1964. With permission from the Royal Society.)

Deborah numbers much closer to unity, falling between solids and fluids. Silly putty® (Binney & Smith, Easton, Pennsylvania, U.S.) provides a classic example of a viscoelastic material. It bounces elastically in response to the short but high strain rate of hitting the floor. When left on a table, however, the long but low strain rate of gravity results in flow. Fracture of viscoelastic materials can often be approximated using linear elastic fracture mechanics, but the approximation applies only over the limited range of strain rates and timescales under which elastic behaviour dominates viscous behaviour (Anderson 1995).

Granular materials Clean, coarse sands such as those found on wave-swept beaches behave differently from more continuous solids. Mechanical behaviour of granular materials depends on particle size, surface characteristics, heterogeneity and packing structure, as well as the viscosity of the interstitial fluid and the length scale being studied (Duran 2000, Goldenberg & Goldhirsch 2005). Extensive research on granular materials has focused on materials composed of large (e.g., 1 mm), noncohesive grains in air, for which environmental influence (e.g., viscosity of the surrounding fluid) is minimal (Duran 2000). Granular materials, when agitated at high frequency, behave like molecules in a fluid. When particles are not agitated, they can still flow under shear, but only in distinct layers lacking the smooth velocity gradient of a fluid (e.g., a snow avalanche). The stochastic behaviours of granular materials result in part from randomness in contacts between particles. In a triangular packing scheme, an individual particle contacts six other particles, but it only needs two contacts below the centre of gravity to be stable. Stress in a granular material follows random chains of particles, such that some particles bear a disproportionate fraction of the load applied to the material, while others bear little or none

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Figure 6 Light-coloured stress chains in a 2-D granular medium (of birefringent disks) visualized using photoelastic stress analysis. (A) stress resulting from gravity; (B) stress resulting from a point force on the surface; (C, D) stress resulting from a point force with stress from gravity subtracted using two different methods (From Geng et al. 2001. With permission from the American Physical Society.)

(Figure 6) (e.g., Geng et al. 2001). Stress chains form arches that can block flow of granular materials through narrow discharge orifices, causing problems for distribution of grain and gravel, for example. A vertical stress is redirected laterally to varying extents depending on packing structure, which in turn depends on size and shape distributions of grains. Granular materials exhibit a nonlinear stress-strain relationship because as stress increases, particle packing changes, resulting in more contacts and increased rigidity (Duran 2000). Under shear, tightly packed particles exhibit dilatancy. When walking on a beach, footprints appear dry, a phenomenon first identified by Reynolds. When particles are tightly packed, they fill a minimal volume. In order to deform and begin to flow under shear, particles must move to a less tightly packed configuration, increasing the volume of the material. The footprint on a beach appears dry because shear exerted by the foot causes the sand grains to separate, the volume to expand and the water to drain downward into the expanded interstices. A minimal packing density exists for dilatancy to occur; less tightly packed particles move under shear without volume expansion (Jaeger & Nagel 1992). Fracture patterns have been observed in granular materials, generally following force arches. In a falling stack of grains, fracture patterns are visible below force arches holding the overlying grains. Fractures generally begin at a wall, suggesting that friction against the wall holds the force arch in place while the underlying grains fall away. Additionally, fracture occurs around a larger grain moving upward in a bed of smaller grains by vibration (Duran 2000). Behaviours of granular materials become more complex as grain sizes decrease, viscous forces begin to become important, and adhesive and cohesive forces become relatively stronger relative to grain weight. Behaviours depend on the scale of the material as well. Bulk granular material containing a large enough number of particles can be considered a continuum, a simplification that fails on a more local level. Increased friction of grains causes granular materials to behave more

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elastically, but only on a large enough spatial scale; on a smaller scale, characteristic stress chains dominate the mechanics (Goldenberg & Goldhirsch 2005).

Bulk mechanical properties of sediments at burrowing-relevant scales Grain-scale structures of sediments have been discussed to foster some intuition about why bulk sediments behave mechanically as they do and because it is likely that bulk properties of sediments will soon be predictable from them (Torquato 2001). For the remainder of the review, however, the focus is on bulk properties. The justification again is a simple scaling argument, i.e., that the burrowers are many times the length scale of the grains. The polymeric organic material in mud, when separated from the grains, shows elastic behaviour. Frankel & Mead (1973) separated the organic material from the grains and observed meiofauna moving through the material on a depression slide. After animals moved through the material, the clumps returned elastically to their original shapes and positions. The clump of material through which the animal was moving would commonly be moved in the direction of the animal’s motion, but more slowly than the animal. They suggest that the response of the mucilaginous material indicates both ‘viscous, and elastic’ elements, but the ‘viscous’ response is likely an artifact of detaching the material from the sediment grains and putting it in a depression slide. This elastic behaviour was recently confirmed through work on methane bubble growth and movement (Johnson et al. 2002). Bubbles injected in sediment are crack-shaped rather than spherical, with aspect ratios predicted by linear elastic fracture mechanics (LEFM) (Johnson et al. 2002, Boudreau et al. 2005). The small forces exerted by the surface tension and buoyancy of bubbles can propagate cracks in mud (Figure 7) (Johnson et al. 2002, Boudreau et al. 2005). The internal pressure required for crack propagation (Pc) by a bubble of volume V depends on the critical stress intensity factor (KIc) and elastic (Young’s) modulus (E) as 1

 1 6 K Ic π    12  6 5

Pc =

4 5

1 5

E V

1 5

(1)

(Johnson et al. 2002). While KIc, the material property governing fracture, is much more important than E in determining critical pressure, the aspect ratio of the bubble (bc/ac) depends much more strongly on E, as bc K Ic π = ac E ac

(2)

Although mud is elastic on the temporal and spatial scales of bubbles, it will flow when small forces are exerted over long periods (e.g., by gravity), demonstrating viscoelastic behaviour. For forces exerted over short intervals the material behaves elastically but over longer periods, viscous properties and creep may need to be considered, particularly for high-porosity muds. If a material creeps when under constant displacement, the elastic restoring force decreases over time, resulting in loss of elastic potential energy and permanent deformation. Beyond the limit of elastic behaviour,

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Figure 7 (A, B) A high-resolution CAT-scan of a bubble injected into sediment from Cole Harbor, Nova Scotia. The bright object is the injection capillary, and the sediment has been made transparent. The bubble is about 20 mm across and 0.7 mm thick, with a resulting volume of 300 mm3. The sample is from the 25–35 cm depth interval of this core. (C, D) plan and cross-sectional views of a bubble rising in doublestrength gelatin. The bubble is 38 mm wide and 1 mm thick. (From Boudreau et al. 2005. With permission from The Geological Society of America.)

plastic deformation occurs. Although plastic deformation is not important for bubbles, it is likely to be more important on the larger scales of animals. LEFM accurately predicts the aspect ratio of bubbles in sediment and gelatin (a clear analogue with similar E and KIc) (Johnson et al. 2002, Boudreau et al. 2005), but some animals exert a much larger displacement than observed with bubbles. If the aspect ratio is larger than predicted by LEFM, the material is behaving nonlinearly, and significant plastic deformation or creep may occur. Marine sediments exhibit both thixotropic and dilatant properties (Chapman 1949). The term thixotropy, originally used to describe the isothermal, reversible gel-sol transition of colloids, has been generalised to include changes in load-deformation behaviour with time, specifically a decrease in viscosity with increased rate of shear or with time under a constant shear (Chapman 1949, Santamarina et al. 2001). Thixotropic behaviour results from the breakdown of the polymeric matrix among particles, but the exact mechanism is unknown. Dilatancy has been described as an increase in resistance with increased shear (Chapman 1949), but more accurately refers to an increase in volume due to expansion of pore space when particles begin to move (Duran 2000). Whereas shear decreases particle contacts, a direct pressure increases the number of grain contacts and, consequently, resistance to penetration. Thus, dilatancy is a mechanism that could be used to reduce the force required for burrowing, and exertion of shear rather than normal stress should be a more efficient burrowing mechanism in sands. Granular materials such as sands exhibit dilatant behaviour, whereas thixotropy is characteristic of viscoelastic materials, or muds.

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Grain size

Granular (Transitional) Elastic

Viscoelastic

Str de ain-r sh pend ate ea r fo ent rce s

Ad Co hesi he on sio an d n

Gr av ity

KELLY M. DORGAN, PETER A. JUMARS, BRUCE D. JOHNSON & BERNARD P. BOUDREAU

Viscous

Porosity

Figure 8 Conceptual diagram outlining dependence of mechanical behaviour on grain size and porosity of marine sediments. The ellipse encompasses the range of grain sizes and porosities found in natural sediments. Sands behave like granular materials, muds like elastic solids, and resuspended fluid mud layers viscously. A transition zone exists between sands and muds in which gravitational forces at grain contacts are comparable with adhesive forces between the polymeric matrix and grains. Sand grains within a matrix of fine grains and polymers likely fall within this transition zone. At the other end, muds that are highly porous but not resuspended behave viscoelastically.

In muds, the polymeric matrix surrounding grains dominates mechanical behaviour. Sands on wave-swept beaches fall on the other end of the continuum, behaving like dry, granular materials. The field of granular mechanics reveals why a transition from granular mechanics to solid mechanics might be expected as grain size decreases (Figure 8). The weight of an individual large sand grain is sufficient to bring it into contact with its neighbours below, and the transmitted forces are large compared with the adhesive forces of the organic polymers connecting grains. It is not yet clear where in terms of grain size or other characteristics the transition from granular mechanics to viscoelastic mechanics occurs. What is apparent, from the limited measurements made to date (Boudreau, unpublished data), is that even fairly coarse silts with considerable sand content behave more or less elastically. That is, elastic or viscoelastic behaviour dominates below the sand-silt grain size transition (70 m and is seldom found between 50 and 70 m, except for in seamounts or upwelling systems (Ballesteros, unpublished data). Moreover, recent (1999) large-scale mortality events of benthic suspension feeders thriving in coralligenous communities have been attributed to unusually long-lasting periods of high temperatures during summer (Perez et al. 2000; Romano et al. 2000), although the ultimate cause of these mortalities remains unclear (possible causes include high temperatures, low food availability, pathogens and physiological stress).

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0 14

10

16 18 20 17 19 15

22 21

21

20 19 18 17

16

14

13

22

20

depth (m)

30 40 50 60 70 80

12.5

J

13

12.5

F

M

A

13.5

M

J

J

A

14

S

15

O

14 13.5

N

D

Time

Figure 6 Average seawater temperatures for a depth of between 0 and 80 m off the Medes Islands (July 1973–December 1977). Shaded area corresponds to depth of coralligenous outcrops. (From Pascual & Flos, 1984. With permission.)

Salinity The relatively shallow and coastal coralligenous communities of Banyuls and the Medes Islands experience salinity ranges between 37 and 38 (Laubier 1966, Pascual & Flos 1984), although salinity variations for coralligenous assemblages from insular areas should be lower.

Geographical distribution Coralligenous buildups are common all around the Mediterranean coasts, with the possible exception of those of Lebanon and Israel (Laborel, 1987). According to Laborel (1961), the best developed formations are those found in the Aegean Sea, although the most widely studied banks are those of the northwestern Mediterranean; therefore, most of the data presented here come from this area.

Depth distribution The minimal depth for the formation of coralligenous frameworks depends on the amount of irradiance reaching the sea bottom. On vertical slopes in the area around Marseilles this minimal depth reaches 20 m, but it is much lower in other zones like the Gulf of Fos, where coralligenous communities are able to grow in shallower waters (12 m) because of the high turbidity of the water related to the Rhône mouth. This minimal depth is displaced to deeper waters in insular areas like Corsica or the Balearic Islands, where water transparency is very high (Ballesteros & Zabala 1993). However, coralligenous frameworks can appear in very shallow waters if light conditions are dim enough to allow a significant development of coralline algae (Laborel 1987, Sartoretto 1994) and they may even occur in the clearest waters like those around Cabrera, where they can be found at a depth of only 10 m in a cave entrance (Martí et al. 2004). The depth distribution of coralligenous assemblages in subhorizontal to horizontal bottoms for different Mediterranean areas is summarised in Table 1.

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Table 1 Depth intervals for the distribution of coralligenous outcrops in different Mediterranean areas Region

Depth (m)

Banyuls Marseilles Medes Islands Tossa de Mar Naples Cabrera Corsica Northeastern Mediterranean Aegean Islands Siculo-Tunisian area Southeastern Mediterranean

20–40 20–50 20–55 20–60 45–70 50–100 60–80 70–90 90–110 90–120 100–120

Reference Feldmann 1937, Laubier 1966 Laborel 1961, Hong 1980 Gili & Ros 1984 Ballesteros 1992 Bacci 1947 Ballesteros et al. 1993 Laborel 1961 Laborel 1961 Laborel 1961 Laborel 1961 Laborel 1961

Structure Coralligenous types: structure and habitats The morphology and inner structure of coralligenous frameworks depends greatly on depth, topography, and the nature of prevailing algal builders (Laborel 1961). Two main morphologies can be distinguished (Pérès & Picard 1964, Laborel 1987): banks and rims. Banks are flat frameworks with a variable thickness that ranges from 0.5 to several (3–4) m. They are mainly built over more or less horizontal substrata, and have a very cavernous structure (numerous holes, Laborel 1987) that often leads to a very typical morphology (it has been compared to Gruyère cheese) (Figure 7A). These banks are sometimes surrounded by sedimentary substrata, and Pérès & Picard (1952) argued that they developed from the coalescence of rhodoliths or maërl (coralligène de plateau). However, it is highly probable that these frameworks have almost always grown upon rocky outcrops (Got & Laubier 1968, Laborel 1987) (Figure 7B). Rims develop in the outer part of marine caves and on vertical cliffs, usually in shallower waters than banks. The thickness of rims is also variable and ranges from 20–25 cm to >2 m; thickness increases from shallow to deep waters (Laborel 1987) (Figure 7C). In shallow water the main algal builder is Mesophyllum alternans, which builds flat or slightly rounded banks or rims with a foliaceous structure. As the water deepens, other corallines (Lithophyllum frondosum, L. cabiochae, Neogoniolithon mamillosum) become important builders. Shallow water banks are generally covered with populations of green algae Halimeda tuna and Flabellia petiolata (Lithophyllo-Halimedetum tunae), which can be so dense that they hide the calcareous algae. However, at greater depths the density of these erect algae decreases and corallines dominate the community (Rodriguezelletum strafforellii). Holes and cavities within the coralligenous structure always sustain a complex community dominated by suspension feeders (sponges, hydrozoans, anthozoans, bryozoans, serpulids, molluscs, tunicates) (Figure 7D). The smallest crevices and interstices of the coralligenous buildup have an extraordinarily rich and diverse vagile endofauna of polychaetes and crustaceans, while many attached or unattached animals cover the main macroalgae and macrofauna, swarm everywhere, from the surface to the cavities or inside the main organisms, and thrive in the small patches of sediment retained by the framework.

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Figure 7 (See also Colour Figure 7 in the insert following page 276.) Types and habitats in coralligenous outcrops. (A) small coralligenous accretion apparently developed from the coalescence of rhodoliths (Tossa de Mar, NE Spain, 40 m depth); (B) coralligenous bank grown upon a rocky outcrop (Tossa de Mar, NE Spain, 25 m depth); (C) community dominated by suspension feeders in a coralligenous cavity (Cabrera, Balearic Islands, 52 m depth); (D) coralligenous rim on a vertical cliff (Gargalo, Corsica, 48 m depth). (Photos by the author.)

According to Hong (1982) four different categories of invertebrates can be distinguished with respect to their position and ecological significance in the coralligenous structure: 1. Fauna contributing to buildup, which help develop and consolidate the framework created by the calcareous algae. Several bryozoans, polychaetes (serpulids), corals and sponges constitute this category. They include 24% of the total species number. 2. Cryptofauna colonising the small holes and crevices of the coralligenous structure. They represent around 7% of the species, including different molluscs, crustaceans and polychaetes. 3. Epifauna (living over the concretions) and endofauna (living inside the sediments retained by the buildup), which represent a great number of species (nearly 67%). 4. Eroding species, accounting for only around 1%.

Algal builders Coralline algae are the main coralligenous builders (Laborel 1961, Laubier 1966, Sartoretto 1996). The taxonomy of this group of algae is very difficult to determine and the nomenclature of the 134

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Figure 8 (See also Colour Figure 8 in the insert.) Main red algal building species in coralligenous frameworks. (A) Mesophyllum alternans; (B) Lithophyllum frondosum; (C) Lithophyllum cabiochae; (D) Neogoniolithon mamillosum; (E) Peyssonnelia rosa-marina. (Photos by the author.)

species is constantly changing. Due to their great importance in the construction of coralligenous frameworks several issues regarding the taxonomic status and current nomenclature of the main species are considered here. The main algal building species, according to Sartoretto (1996) and several other authors (e.g., Feldmann 1937, Pérès & Picard 1964, Boudouresque 1970, Hong 1980, Ballesteros 1991b), has repeatedly been identified as Mesophyllum lichenoides (Ellis) Lemoine. However, Cabioch & Mendoza (1998) reported the most common species of the genus Mesophyllum growing in coralligenous assemblages to be a different species and named it Mesophyllum alternans (Foslie) Cabioch & Mendoza (Figure 8A). Although present in the Mediterranean Sea, M. lichenoides does not seem to contribute to coralligenous buildup (Cabioch & Mendoza 1998). Therefore, it is likely that some or most of the reports of M. lichenoides as a coralligenous builder actually refer to M. alternans (Cabioch & Mendoza, 1998) (Figure 8A). Pseudolithophyllum expansum (sensu Lemoine) has been identified by most authors as being the second most common coralline alga in coralligenous concretions. However, Boudouresque & Verlaque (1978) identified another species, similar to P. expansum, and described it as P. cabiochae. Later, studies by Woelkerling (1983), Athanasiadis (1987), Woerkerling et al. (1993) and Furnari 135

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et al. (1996) shed some light (but also added further confusion) regarding the name to be applied to the alga called P. expansum and/or P. cabiochae by Mediterranean phycologists and marine biologists. The last review by Athanasiadis (1999a) suggested that Pseudolithophyllum should not be regarded as a different genus to Lithophyllum and that the two species growing in coralligenous communities should be named Lithophyllum stictaeforme (Areschoug) Hauck [= Lithophyllum frondosum (Dufour) Furnari, Cormaci & Alongi; = Pseudolithophyllum expansum (Philippi) Lemoine; = Lithophyllum expansum sensu Lemoine] (Figure 8B) and Lithophyllum cabiochae (Boudouresque & Verlaque) Athanasiadis (Figure 8C). However, according to Marc Verlaque (personal communication), L. stictaeforme and L. frondosum are not synonyms and the species usually reported as Pseudolithophyllum expansum by Mediterranean phycologists should be named Lithophyllum frondosum. Moreover, Woelkerling (1983) recognised the lectotype of Lithophyllum expansum Philippi (non Lemoine) as a Mesophyllum and considered it to be a heterotypic synonym of M. lichenoides. However, a recent study by Cabioch & Mendoza (2003) showed that the lectotype of Lithophyllum expansum Philippi is specifically different from Mesophyllum lichenoides, M. alternans and other Mediterranean species of this genus. They named it Mesophyllum expansum (Philippi) Cabioch and Mendoza and it corresponds to the taxa usually identified as Mesophyllum lichenoides var. agariciformis (Pallas) Harvey by Mediterranean phycologists. As a result of all this confusion it is not possible to determine the extent to which M. expansum contributes to coralligenous buildup, although it is likely to make a significant contribution, at least in some places. Another species, Mesophyllum macroblastum (Foslie) Adey, has been reported for the coralligenous frameworks in Corsica (Cabioch & Mendoza 2003), and a fifth species (Mesophyllum macedonis Athanasiadis) (Athanasiadis 1999b) may also be present in the coralligenous frameworks of the Aegean Sea. According to Marc Verlaque (personal communication), three species of the genus Mesophyllum coexist in the coralligenous communities off Marseille (M. alternans, M. expansum, M. macroblastum), suggesting a much greater biodiversity of coralligenous coralline algae than expected. The alga identified by Feldmann (1937) as Lithophyllum hauckii (Rothpletz) Lemoine, a very common coralline in the coralligenous buildups of the Banyuls region, should be named Neogoniolithon mamillosum (Hauck) Setchell & Mason (Hamel & Lemoine 1953, Bressan & BabbiniBenussi 1996) [= Spongites mamillosa (Hauck) Ballesteros] (Figure 8D). Although not a coralline alga, it should also be pointed out that authors prior to 1975 identified the calcareous Peyssonnelia growing in coralligenous communities as being Peyssonnelia polymorpha (Zanardini) Schmitz. Boudouresque & Denizot (1975) described a similar species, Peyssonnelia rosa-marina (Figure 8E), that is more common than P. polymorpha and which also contributes to coralligenous frameworks. Therefore, reports of P. polymorpha prior to the description of P. rosa marina should probably be regarded as referring to this latter species or to both entities. Feldmann (1937) identified the four main calcareous algae responsible for the coralligenous frameworks in the region of Banyuls: Lithophyllum frondosum (as Pseudolithophyllum expansum), Neogoniolithon mamillosum (as Lithophyllum hauckii), Mesophyllum alternans (as M. lichenoides) and Peyssonnelia rosa-marina f. saxicola (as P. polymorpha). The same species have also been reported for coralligenous frameworks studied in several areas close to the Gulf of Lions (e.g., Boudouresque 1973, Ballesteros 1992). It seems that these species are almost always the same, with the possible exception of Lithophyllum frondosum which seems to be replaced by L. cabiochae in several areas of the Mediterranean that are warmer than the Gulf of Lions (e.g., Corsica, Balearic Islands, the eastern Mediterranean). Hong (1980) reports three species as being the main coralligenous builders in the region of Marseilles: Lithophyllum cabiochae, Mesophyllum alternans (?) and Neogoniolithon mamillosum. Peyssonnelia rosa-marina is also very abundant. Other calcareous species contributing to buildup are Archaeolithothamnion mediterraneum, Lithothamnion sonderi (?) and Peyssonnelia polymorpha. 136

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According to Sartoretto et al. (1996), Mesophyllum alternans (as M. lichenoides) is the main algal building species for both ancient and recent coralligenous constructions in the northwestern Mediterranean. Mesophyllum alternans is a highly tolerant species in terms of light, temperature and hydrodynamism, and is currently the dominant species in shallow waters. In some areas, Peyssonnelia rosa-marina and P. polymorpha may also be the dominant species, and form a very cavernous, highly bioeroded coralligenous framework. In deep waters Lithophyllum cabiochae is the main calcareous alga in the region of Marseilles and Corsica, but its cover can vary from one geographical area to another. For example, the encrusting algal cover in deep-water coralligenous frameworks in Marseilles is limited to a few isolated small living thalli that seem insufficient to allow current renewal of the coralligenous construction. In contrast, these deep frameworks are luxuriant in Corsica, as evidenced by the accumulation of living thalli of L. cabiochae. The identification of the species present in the algal framework of coralligenous blocks from 7700 years ago to the present has shown that no species changes have occurred (Sartoretto et al. 1996). The study by Sartoretto et al. (1996) in the Marseilles region and Corsica identified five Corallinaceae and one Peyssonneliaceae: the nongeniculate corallines Mesophyllum alternans (as M. lichenoides), Lithophyllum sp. (as Titanoderma sp., probably Lithophyllum pustulatum v. confinis), Lithophyllum cabiochae-frondosum (discrimination between L. cabiochae and L. frondosum is uncertain in fossil material), Lithothamnion sp., the geniculate coralline alga Amphiroa verruculosa, and, finally, Peyssonnelia sp. Mesophyllum alternans is also the main algal builder in the coralligenous frameworks of the Mediterranean Pyrenees (Bosence, 1985), along with Lithophyllum and Titanoderma (quoted as Pseudolithophyllum and Tenarea in Bosence’s paper). Peyssonnelia polymorpha and P. rosa-marina f. saxicola may also be abundant in the coralligenous frameworks of the Mediterranean Pyrenees, the northeast coast of Spain, and the Balearic Islands (Bosence 1985, Ballesteros 1992, Ballesteros et al. 1993). However, even if Peyssonnelia is abundant as a living encrusting alga, it is almost completely absent from the fossil record (Bosence 1985, Sartoretto 1996). Carbonate content of the Peyssonnelia species is lower than the average carbonate content in corallines (Laubier 1966, Ballesteros 1992), and calcification in the form of aragonite rather than calcite prevents a good fossilization of these species (James et al. 1988). However, these and other species of Peyssonnelia usually have a basal layer of aragonite that may contribute to the consolidation of coralligenous frameworks when mixed with the physico-chemical precipitations of CaCO3 (Sartoretto 1996).

Animal builders Coralligenous animal builders have been studied in the Marseilles region (Hong 1980) where 124 species contribute to the frameworks, and account for around 19% of the total number of species reported. The most abundant animal group are the bryozoans, accounting for 62% of species, followed by the serpulid polychaetes with 23.4%. Minor contributors are the cnidarians (4%), molluscs (4%), sponges (4%), crustaceans (1.6%) and foraminiferans (0.8%). However, Laborel (1987) considers the foraminiferan Miniacina miniacea (Figure 9A) to be the most important animal builder. Hong (1980) distinguished three different types of animal builders: those contributing directly to the framework, and which are relatively large; those with a reduced builder activity due to their small size; and those which agglomerate carbonate particles. The first group includes the bryozoans Schizomavella spp., Onychocella marioni, Cribilaria radiata, Pentapora fascialis, Enthalophoroecia deflexa, Celleporina caminata, Myriapora truncata, Brodiella armata and Turbicellepora coronopus (Figures 9B,C), several serpulids (Serpula vermicularis, S. concharum, Spirobranchus polytrema) (Figure 9D), the molluscs Vermetus sp., Serpulorbis arenarius and Clavagella melitensis, and the scleractinians Hoplangia durotrix, Leptopsammia pruvoti, Caryophyllia inornata and C. smithii (Figure 9E). Among the second group, Hong (1980) reports some small bryozoans 137

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Figure 9 (See also Colour Figure 9 in the insert.) Some animal building species in coralligenous frameworks. (A) Miniacina miniacea; (B) Pentapora fascialis; (C) Myriapora truncata; (D) Serpula vermicularis; (E) Leptopsammia pruvoti. (Photos by the author.)

such as Crassimarginatella maderensis and Mollia patellaria, serpulids like Hydroides spp., Filogranula spp., and Spirorbis spp., the cirripedes Verruca strömia and Balanus perforatus, and the foraminiferan Miniacina miniacea. In terms of the ‘agglomerative’ animals, he reports sponges such as Geodia spp., Spongia virgultosa and Faciospongia cavernosa, the bryozoans Beania spp., and the alcyonarian Epizoanthus arenaceus.

Bioeroders Feldmann (1937) described the abundance of several organisms that erode calcareous concretions, in particular the excavating sponge Cliona viridis (Figure 10A), the bivalve Lithophaga lithophaga and several annelids. Hong (1980) listed 11 bioeroders in the coralligenous communities of Marseilles: four species of sponges of the genus Cliona, three species of molluscs, two species of polychaetes of the genus Polydora and two sipunculids. According to Sartoretto (1996), the organisms that erode coralligenous frameworks are similar to those eroding other marine bioherms such 138

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Figure 10 (See also Colour Figure 10 in the insert.) Bioeroders in coralligenous frameworks. (A) Cliona viridis; (B) Sphaerechinus granularis; (C) Echinus melo; (D) browsing marks of Sphaerechinus granularis over Lithophyllum frondosum. (Photos by the author.)

as the trottoir of Lithophyllum byssoides or the coral reefs. Three types of eroding organisms can be distinguished: browsers, microborers and macroborers. The only browsers in the coralligenous concretions are sea urchins (Laubier 1966), because the only important Mediterranean fish grazing on algae (Sarpa salpa) do not usually thrive in coralligenous communities. Sphaerechinus granularis (Figure 10B,D) is an important biological agent that substantially erodes coralligenous concretions, although local variations in sea urchin abundance and individual size greatly influence the amount of calcium carbonate eroded annually. Another sea urchin commonly found in coralligenous communities is Echinus melo (Figure 10C). The proportion of calcareous algae in its digestive content ranges from 18–50% of the total (Sartoretto 1996) and it preys mainly on sponges, bryozoans and serpulid polychaetes. Given the low densities of this sea urchin in coralligenous communities (1–3 individuals in 25 m2), Sartoretto (1996) concludes that the bioerosional role of E. melo is very limited. Microborers include blue-green algae (cyanobacteria), green algae and fungi (Hong 1980). Three green algae (Ostreobium quekettii, Phaeophila sp. and Eugomontea sp.) and four cyanobacteria (Plectonema tenebrans, Mastigocoleus testarum, Hyella caespitosa and Calothrix sp.), together with some unidentified fungi, seem to be the main microborers in coralligenous communities. Diversity is higher in shallow waters, whereas, according to colonisation studies conducted by Sartoretto (1998), it is restricted to only one species (Ostreobium) in deep waters (>60 m). Macroborers comprise molluscs (Lithophaga lithophaga, Gastrochaena dubia, Petricola lithophaga, Hyatella arctica), sipunculids (Aspidosiphon mülleri, Phascolosoma granulatum), polychaetes (Dipolydora spp., Dodecaceria concharum) and several excavating sponges (Sartoretto 1996, Martin & Britayev 1998). Among perforating sponges commonly found in coralligenous communities, some of them excavate mainly in Corallium rubrum and other calcareous cnidarians (Aka labyrinthica, Scantilletta levispira, Dotona pulchella spp. mediterranea, Cliona janitrix), whereas others, such as Pione vastifica, Cliona celata, C. amplicavata, C. schmidtii and C. viridis can be 139

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found in a wide range of calcareous substrata (coralline algae, bivalves, madreporids, etc.) (Rosell & Uriz 2002). Cliona viridis is the most powerful destructive sponge of calcareous substrata (Rosell et al. 1999), and is the most abundant excavating sponge in coralligenous communities (Uriz et al. 1992a). The encrusting sponges and the Sipunculida become more abundant in polluted coralligenous environments (Hong 1983).

Assemblages The final result of the builders and eroders of coralligenous concretions is a very complex structure, in which several microhabitats can be distinguished (Figure 11). Environmental factors (e.g., light, water movement and sedimentation rates) can vary by one to two orders of magnitude in parts of the same concretion situated as close as one metre from each other. This great environmental heterogeneity allows several different assemblages to coexist in a reduced space. For practical purposes those situated in open waters (from horizontal to almost vertical surfaces) are distinguished here from those situated in overhangs and cavities. The assemblages of macroborers are not discussed because the only available data have already been commented on, nor are the assemblages thriving in the patches of sediment between or inside coralligenous frameworks because there are no quantitative data on them. Algae, both encrusting corallines and green algae, usually dominate in horizontal to subhorizontal surfaces (Figure 12), although their abundance decreases with depth or in dim light. Phycologists have distinguished two main communities according to the light levels reaching coralligenous frameworks. In shallower waters Mesophyllum alternans usually dominates in the basal layer and Halimeda tuna in the upper stratum, with an important coverage of other algae (Peyssonnelia spp., Flabellia petiolata) (Figure 13A). This plant association has received the name of LithophylloHalimedetum tunae, and has been described in detail by Ballesteros (1991b). Algal biomass ranges between 1200 and 2100 g dry weight (dw) m–2, while percent cover ranges from 180–400%. The number of species is very high (average of 76 species in 1024 cm2) and average diversity is 2.5 bits ind–1. Its bathymetric distribution ranges from a depth of 12–15 m to 30–35 m in the Gulf of Lions, but it can reach depths below 50 m in the clear waters of seamounts and insular territories of the western and eastern Mediterranean. This association develops at irradiances ranging from around

Figure 11 (See also Colour Figure 11 in the insert.) Diagrammatic section of a coralligenous bank, showing the high small-scale environmental heterogeneity and the different microhabitats. (Drawing by J. Corbera.)

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Figure 12 (A) Drawing of a coralligenous concretion dominated by algae in the Medes Islands (NE Spain).

2.3–0.3 W m–2, which correspond, respectively, to 3 and 0.4% of the surface irradiance. Other quantified species lists are described in Marino et al. (1998). In deeper waters or lower irradiances the density of Halimeda tuna decreases and other calcareous algae become dominant (Lithophyllum frondosum, Neogoniolithon mamillosum, Peyssonnelia rosa-marina) (Figure 14). Other common algae are members of the family Delesseriaceae 141

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Figure 12 (continued) (B) Key to major species, on the left from top to bottom: Alcyonium acaule16, Crambe crambe on Spondylus gaederopus28, Cystodites dellechiajei31, Myriapora truncata23, Microcosmus sabatieri33, Hemimycale columella9, Sertularella ellisi13, Ophiothrix fragilis30, amid Halimeda tuna (a close up is shown at bottom left with, on it4, Titanoderma sp.6, Halecium halecinum14, Campanularia sp.15, Aetea truncata24, Watersipora subovoidea25 and Polycera quadrilineata26 with spawn mass27 below). At the centre and to the right, from top to bottom, and in addition to the abovementioned species: Eunicella singularis17, Codium bursa1, Codium vermilara5, Cliona viridis10, Pentapora fascialis22, Salmacina dysteri20, Scorpaena porcus34, Sabella sp.21, Parazoanthus axinellae18, Peyssonnelia rubra2, Oscarella lobularis7, Ircinia variabilis8, Caryophyllia sp.19, Palaemon serratus29, Conger conger35, Botryllus schlosseri32, Agelas oroides12, Crambe crambe11 and Sciaena umbra36, all amid Flabellia petiolata3. (Drawing by M. Zabala in Els Sistemes Naturals de les Illes Medes, Ros et al., 1984. With permission from M. Zabala and J. Ros.)

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Figure 13 (See also Colour Figure 13 in the insert.) Different assemblages of algal-dominated coralligenous banks and rims; (A) with Halimeda tuna and Mesophyllum alternans (Tossa de Mar, NE Spain, 28 m depth); (B) with Lithophyllum frondosum (Tossa de Mar, NE Spain, 40 m depth); (C) with Peyssonnelia rosa-marina, Mesophyllum alternans, Palmophyllum crassum and Peyssonnelia squamaria (Scandola, Corsica, 50 m depth); (D) detail of C. (Photos by the author.)

and other laminar red algae (Kallymenia, Fauchea, Sebdenia, Rhodophyllis, Predaea), as well as the encrusting green alga Palmophyllum crassum. These assemblages correspond to the Rodriguezelletum strafforellii of Augier & Boudouresque (1975), which may be identical to the algal assemblage described by Feldmann (1937) for coralligenous concretions from the Mediterranean Pyrenees (Figures 13B,C,D). Quantified species lists can be found in Boudouresque (1973), Augier & Boudouresque (1975), Ballesteros (1992) and Marino et al. (1998). Algal biomass averages 1600 g m–2 and percent cover 122%, mostly corresponding to encrusting algae and, around 90%, corresponding to corallines; the number of species is low (38 species in 1600 cm2 or lower) (Ballesteros 1992). Animal assemblages of these two plant associations can differ greatly from one to the other, as well as between sites and geographical areas. The abundance of suspension feeders mainly depends on average current intensity and availability of food (plankton, POC, DOC). In the richest zones (e.g., Gulf of Lions, Marseilles area) gorgonians can dominate the community (Figure 15A,B), but in very oligotrophic waters (e.g., Balearic Islands, eastern Mediterranean), sponges, bryozoans and small hexacorals are the dominant suspension feeders (Figure 15C). The only available quantified biomass data of invertebrate assemblages are those of True (1970) gathered from the Marseilles area, and those results are summarized below. True (1970) studied an assemblage dominated by Eunicella cavolinii. He reports a basal layer of encrusting algae accompanied by erect algae (total biomass of 163 g dw m–2). E. cavolinii is the most abundant species (up to 304 g dw m–2), followed by the bryozoans Pentapora fascialis (280.1 g dw m–2), Turbicellepora avicularis (49.1 g dw m–2), Celleporina caminata (22.3 g dw m–2) and Myriapora truncata (19.9 g dw m–2). Other less abundant species include unidentified Serpulidae, anthozoans Parerythropodium coralloides, Alcyonium acaule, Leptopsammia pruvoti and 143

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Figure 14 (See also Colour Figure 14 in the insert.) (A) Drawing of a deep-water, animal-dominated, coralligenous assemblage in the Medes Islands (NE Spain).

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Figure 14 (continued) (See also Colour Figure 14 in the insert.) (B) Key to major species, left from top to bottom: Paramuricea clavata6, (and on it Halecium halecinum12, Pteria hirundo22), Aglaophenia septifera14, Cliona viridis7, Alcyonium acaule17, Acanthella acuta11, Lithophyllum frondosum1, Agelas oroides6, Palinurus elephas24, Parazoanthus axinellae19, Spirastrella cunctatrix9, Chondrosia reniformis5, Petrosia ficiformis4 (and on it Smittina cervicornis27 and Discodoris atromaculata23), Serpula vermicularis21, Caryophyllia inornata20, Halocynthia papillosa28, Clathrina coriacea3, Corallium rubrum18 and Chromis chromis.32 Right, from top to bottom (excluding the above-mentioned species): Anthias anthias31, Eunicella singularis15, Diplodus sargus29, Codium bursa8, Epinephelus marginatus30, Phyllangia mouchezii26, Galathea strigosa25, Synthecium evansi13, Dysidea avara10. (Drawing by M. Zabala & J. Corbera.)

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Figure 15 (See also Colour Figure 15 in the insert.) Different assemblages of animal-dominated coralligenous banks and rims; (A) with gorgonians Paramuricea clavata and Eunicella cavolinii but also green algae Halimeda tuna and Flabellia petiolata (Gargalo, Corsica, 45 m depth); (B) with Paramuricea clavata and encrusting sponges in deep waters (Cabrera, Balearic Islands, 65 m depth); (C) with sponges, bryozoans and anthozoans (Cabrera, Balearic Islands, 50 m depth); (D) overhangs with Corallium rubrum (Palazzu, Corsica, 35 m depth). (Photos by the author.)

Caryophyllia smithii, tunicates Microcosmus polymorphus and Halocynthia papillosa, foraminiferan Miniacina miniacea, sponges Chondrosia reniformis and Axinella damicornis and other bryozoans (Adeonella calveti, Beania hirtissima, Sertella spp., Schizomavella spp. and Cellaria salicornioides). The number of collected invertebrate species amounted to 146 in 7500 cm2, with a total weight of invertebrates close to 1563 g dw m–2. The main biomass corresponded to the phylum Bryozoa, closely followed by Cnidaria, and, with much lower values, Annelida, Porifera, Chordata (tunicates) and Mollusca. Another assemblage studied by True (1970) is that dominated by Paramuricea clavata. Populations of P. clavata are abundant in steep rocky walls, but they also grow in horizontal to subhorizontal surfaces if light levels are very low. The basal layer of the community can be mainly occupied by algae (usually attributable to Rodriguezelletum strafforellii association) or by other suspension feeders (sponges and bryozoans). The lists of True (1970) do not report any algae. Paramuricea clavata has a total biomass of 746 g dw m–2, followed by the cnidarians Caryophyllia smithii (326.3 g dw m–2) and Hoplangia durotrix (188.1 g dw m–2), the bryozoan Celleporina caminata (119.6 g dw m–2), the anthozoan Leptopsammia pruvoti (54.9 g dw m–2), the bryozoans Adeonella calveti (32.8 g dw m–2) and Turbicellepora avicularis (31.4 g dw m–2), and red coral (Corallium rubrum, 16.9 g dw m–2). Other less abundant species include unidentified Serpulidae, sponges Ircinia variabilis (fasciculata in True, 1970), Spongia officinalis, Sarcotragus spinosula, Cacospongia scalaris, Petrosia ficiformis, Aplysina cavernicola, Erylus euastrum and Agelas oroides, the bryozoan Sertella septentrionalis, the alcyonarian Parazoanthus axinellae, molluscs Pteria hirundo, Serpulorbis arenarius, Lithophaga lithophaga and Anomia ephippium, and tunicates Microcosmus polymorphus and Polycarpa pomaria. The number of collected invertebrate species 146

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amounts to 111 in 7500 cm2, with a total weight of 3175 g dw m–2. The main biomass corresponds to the phylum Cnidaria, followed by Annelida, Bryozoa, Porifera, Mollusca and Chordata. Gili & Ballesteros (1991) described the species composition and abundance of the cnidarian populations in coralligenous concretions around the Medes Islands that are dominated by the gorgonian Paramuricea clavata. Total cnidarian biomass amounted to 430 g dw m–2, with 13 species of hydrozoans and 9 species of anthozoans found in an area of 5202 cm2. Species contributing the most to the total biomass of the taxocoenosis were the anthozoans Paramuricea clavata, Leptopsammia pruvoti, Parazoanthus axinellae, Caryophyllia inornata, C. smithii, Alcyonium acaule and Parerythropodium coralloides, the hydrozoans Sertularella gaudichaudii and Halecium tenellum also being abundant. Overhangs and big cavities of coralligenous assemblages have a different species composition to that found in open waters (Figure 15D). Algae are usually completely absent because light is very reduced. However, some thalli of encrusting corallines, Peyssonnelia spp. and Palmophyllum crassum, can occasionally be found. There are no quantified species lists for this kind of habitat reported in the literature except for those of True (1970), which, in fact, do not come from a coralligenous buildup but from a semidark zone dominated by red coral in a cave (Grotte de l’Île Plane). This assemblage is worth describing as it is very similar to those that develop in the overhangs of coralligenous constructions in the northwestern Mediterranean, or in coralligenous communities situated in very deep waters. The assemblage of red coral described by True (1970) is dominated by the cnidarians Corallium rubrum (2002 g dw m–2), Caryophyllia smithii (303 g dw m–2), Hoplangia durotrix (54.1 g dw m–2) and Leptopsammia pruvoti (52.4 g dw m–2), the sponges Petrosia ficiformis (241.5 g dw m–2) and Aplysina cavernicola (27.9 g dw m–2), the bryozoan Celleporina caminata (100.5 g dw m–2), and unidentified Serpulidae (232.4 g dw m–2). Other abundant species are the sponges Ircinia variabilis, Spongia officinalis, Aaptos aaptos and Ircinia oros, the molluscs Chama gryphoides and Anomia ephippium, and several unidentified bryozoans. The total number of identified invertebrate species is 63 in 7500 cm2, with a total biomass of 3817 g dw m–2. The dominant phylum is largely the Cnidaria, although Porifera, Annelida and Bryozoa are also abundant. It should be remembered that most of the invertebrate data presented in this chapter, if representative at all, reflect the biomass and species composition of several assemblages of coralligenous buildups from the Gulf of Lions, which are different to those reported from other sites of the western Mediterranean (e.g., Balearic Islands; Ballesteros et al. 1993) or the eastern Mediterranean (Pérès & Picard 1958, Laborel 1960). Therefore, these data cannot be extrapolated to the whole Mediterranean.

Biodiversity Coralligenous communities constitute the second most important ‘hot spot’ of species diversity in the Mediterranean, after the Posidonia oceanica meadows (Boudouresque 2004a). However, there appear to be no previous estimates of the number of species that thrive in these coralligenous assemblages. Furthermore, due to their rich fauna (Laubier 1966), complex structure (Pérès & Picard 1964, Ros et al. 1985), and the paucity of studies dealing with coralligenous biodiversity, they probably harbour more species than any other Mediterranean community. In fact, coralligenous assemblages are one of the preferred diving spots for tourists due to the great diversity of organisms (Harmelin 1993). Divers are astonished by the high number of species belonging to taxonomic groups as diverse as sponges, gorgonians, molluscs, bryozoans, tunicates, crustaceans or fishes. Moreover, there are innumerable organisms living in these coralligenous communities that cannot be observed by diving, nor without a careful sorting of samples. For example, in a sample of 370 g dw of Mesophyllum from a small coralligenous concretion in the south of Spain, García-Raso 147

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(1988) found 903 specimens of crustaceans, molluscs and polychaetes; other organisms from other groups (pycnogonids, nematodes, echinoderms, sipunculids, sponges, tunicates, small fishes, such as Gobiidae and Blenniidae, as well as hydrozoans and bryozoans) were also abundant, although not quantified. Laubier (1966) was the first author to emphasize the great biodiversity of coralligenous communities and listed 544 invertebrates from coralligenous assemblages in the region of Banyuls. Later, in an exhaustive survey of coralligenous communities around Marseilles, Hong (1980) listed a total of 682 species, while several authors (in Ros et al. 1984) report 497 species of invertebrates in the coralligenous assemblages of the Medes Islands. Estimates of the species richness found in coralligenous communities give a very conservative number of 1241 invertebrates (Table 2). Boudouresque (1973) has estimated that at least 315 species of macroalgae can thrive in Mediterranean sciaphilic communities (the coralligenous type being the most widespread). Finally, there are no estimates of the number of fishes that can be found in coralligenous communities, due to the high mobility of most species of this group, but estimates based on available literature regarding the biology of Mediterranean fishes (e.g., Whitehead et al. 1984–1986, Corbera et al. 1996, Mayol et al. 2000) range between 110 and 125 species. It is very difficult to mention all the species found to date in coralligenous communities, as the existing taxonomic literature is huge and contains many synonyms; this makes it impossible for a nonspecialist in most of the groups to come up with an accurate number of reported species. Nevertheless, an attempt is made at a first, and very conservative, estimate of the total number of species, which amounts to some 1,666 (Table 2). A first step toward increased knowledge of the biodiversity present in coralligenous communities would be to obtain a more accurate estimate of which species have been found and their number. The next section describes the main findings reported for each taxonomic group.

Taxonomic groups Algae At least 315 species of macroalgae thrive in deep-water Mediterranean sciaphilic communities (Boudouresque 1973), and most of them are found in coralligenous concretions. The algal assemblages found here show high biodiversity, with an average of 40 algal species in 600 cm2. Boudouresque (1973) defined the ecological group of algae characteristic of coralligenous concretions (CC or Rodriguezellikon), which (Boudouresque, 1985) comprises 28 species (e.g., Rodriguezella spp., Aeodes marginata, Fauchea repens, Chondrymenia lobata, Gulsonia nodulosa, Polysiphonia elongata, Neogoniolithon mamillosum). However, coralligenous communities are never dominated by this group of species, but rather by other species with a more depth-related widespread distribution, examples being the encrusting corallines Mesophyllum alternans, Lithophyllum frondosum, and L. cabiochae, the green algae Palmophyllum crassum, Flabellia petiolata, Halimeda tuna and Valonia macrophysa, some brown algae such as Dictyota dichotoma, Dictyopteris polypodioides, Spatoglossum solierii, Zonaria tournefortii, Halopteris filicina, Phyllariopsis brevipes, Zanardinia prototypus and Laminaria rodriguezii, and a large number of red algae (several species of Peyssonnelia, Kallymenia, Halymenia, Sebdenia, Predaea, Eupogodon, Myriogramme, Neurocaulon foliosum, Acrodiscus vidovichii, Osmundaria volubilis, Phyllophora crispa, Rhodymenia ardissonei, Acrosorium venulosum, Rhodophyllis divaricata, Hypoglossum hypoglossoides, Polysiphonia banyulensis, Plocamium cartilagineum, Sphaerococcus coronopifolius, Erythroglossum sandrianum, and Aglaothamnion tripinnatum) (Boudouresque 1973, 1985, Ballesteros 1992, 1993). The algal component of coralligenous communities largely consists of Mediterranean endemics, which quantitatively represent between 33 and 48% of the total flora (Boudouresque 1985). 148

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Table 2 Approximate number of species reported from coralligenous communities Group

Totals

Algae Protozoans Sponges

315 61 142

Hydrozoans Anthozoans

55 43

Scyphozoans Turbellarians Nemerteans Polychaetes Sipunculids Echiurids Chitons Prosobranchs Opisthobranchs Bivalves Cephalopods Mites Pycnogonids Copepods Ostracods Cirripedes Phyllocarids Mysids Cumaceans Tanaidaceans Isopods Amphipods Decapods Brachiopods Pterobranchs Bryozoans Crinoids Ophiuroids Echinoids Asteroids Holothurioids Tunicates Fishes

1 3 12 191 3 2 7 61 33 41 3 6 15 54 10 3 1 7 3 2 14 100 56 8 1 171 2 17 14 8 9 82 110

References Boudouresque 1973 Laubier 1966, Hong 1980 Laubier 1966, Hong 1980, Ros et al. 1984, Ballesteros et al. 1993, Ballesteros & Tomas 1999, Rosell & Uriz 2002 Laubier 1966, Ros et al. 1984, Ballesteros et al. 1993, Rosell & Uriz 2002 Laubier 1966, Ros et al. 1984, Ballesteros et al. 1993, Ballesteros & Tomas 1999, Ballesteros, unpublished data Laubier 1966, Hong 1980 Laubier 1966, Hong 1980 Laubier 1966 Martin 1987 Laubier 1966, Hong 1980 Laubier 1966 Hong 1980 Hong 1980 Hong 1980 Hong 1980 Ballesteros & Tomas 1999 Laubier 1966 Hong 1980 Laubier 1966 Laubier 1966 Laubier 1966, Hong 1980 Hong 1980 Hong 1980 Laubier 1966, Hong 1980 Laubier 1966, Hong 1980 Laubier 1966, Hong 1980 Bellan-Santini 1998 García-Raso 1988, 1989 Logan 1979 Laubier 1966 Zabala 1986 Tortonese 1965 Laubier 1966, Tortonese 1965 Tortonese 1965, Laubier 1966, Hong 1980, Ros et al. 1984, Munar 1993, Ballesteros et al. 1993, Ballesteros & Tomas 1999 Tortonese 1965, Laubier 1966, Munar 1993 Tortonese 1965, Laubier 1966, Hong 1980, Ros et al. 1984, Munar 1993, Ballesteros et al. 1993, Ballesteros & Tomas 1999 Ramos 1991 Whitehead et al. 1984–1986, Ballesteros, unpublished data

Coralligenous communities are rich in algal species, although this richness is lower than that found in photophilic or moderately sciaphilic communities (Ballesteros 1992). Ballesteros (1991b) reports 90 species of macroalgae from the coralligenous assemblages of Tossa de Mar, where Mesophyllum alternans and Halimeda tuna dominate, but only 38 in the coralligenous communities from a deep water site (Ballesteros 1992). Piazzi et al. (2004) found small differences between algal assemblages of coralligenous habitats along the coast of Tuscany (Italy). However, algal 149

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populations in coralligenous habitats differ greatly on geographical scales across the whole Mediterranean (Boudouresque 1973) and this is the main reason why, even if the species diversity at one site is rather constant, the overall algal richness of coralligenous habitats — on a Mediterraneanwide scale and covering all depths where they are present — can be huge. Protozoa Fifty-four species of Foraminifera are listed by Hong (1980) in the checklist of species from the coralligenous communities of Marseilles, although none of these species seems to be characteristic of coralligenous habitats. Miniacina miniacea is the most abundant species, and other common species include Massilina secans, Planorbulina mediterranensis, Elphidium crispum and Triloculina rotunda. Laubier (1966) reports six species of Folliculinidae living as epibionts of bryozoans. Porifera Coralligenous communities are very rich in sponges, which grow mainly in the more sciaphilic environments but also in more exposed areas. There are also some species (Clionidae) that are active bioeroders and which excavate the coralline framework. The number of species reported from different well-studied areas is 26 species from Banyuls (Laubier 1966), 78 species from Marseilles (Hong 1980), 48 species from the Medes Islands (Bibiloni et al. 1984), 74 species from Cabrera (Ballesteros et al. 1993), and 24 species from Tossa (Ballesteros & Tomas 1999). The list of sponges reported in all these studies (along with those of True 1970 and Rosell & Uriz 2002) amounts to 142 different species. According to Hong (1980) the following species are characteristic of coralligenous biocoenoses: Axinella damicornis, Acanthella acuta, Hymedesmia pansa, Agelas oroides, Dictyonella pelligera, Haliclona mediterranea, Spongionella pulchella and Faciospongia cavernosa. Other abundant sponges (Laubier 1966, True 1970, Hong 1980, Bibiloni et al. 1984, Ballesteros et al. 1993, Ballesteros & Tomas 1999) are: Cliona viridis, Clathrina clathrus, Oscarella lobularis, Chondrosia reniformis, Phorbas tenacior, Geodia cydonium, Aaptos aaptos, Pleraplysilla spinifera, Dysidea avara, Terpios fugax, Spongia virgultosa, S. agaricina, S. officinalis, Ircinia variabilis, I. oros, Axinella verrucosa, A. polypoides, Diplastrella bistellata, Petrosia ficiformis, Hexadella racovitzai, Cacospongia scalaris, Dictyonella obtusa, Erylus euastrum, Hippospongia communis, Reniera cratera, R. fulva, R. mucosa, Spirastrella cunctatrix, Spongosorites intricatus and Hemimycale columella. The coralligenous communities from the eastern Mediterranean seem to be very rich in sponges (Pérès & Picard 1958) because they are almost devoid of alcyonarians and gorgonians. The most abundant species have already been cited above. Those of the genus Axinella (A. polypoides, A. damicornis, A. verrucosa), Agelas oroides and Petrosia ficiformis (Pérès & Picard 1958) are particularly common. Hydrozoa Laubier (1966) reports 16 hydrozoans from the coralligenous communities of Banyuls but none is listed by Hong (1980). Gili et al. (1984) report 44 species of hydrozoans from the coralligenous and precoralligenous communities of the Medes Islands. According to Laubier (1966) and Gili et al. (1984, 1989) some species of hydrozoans are common on deep-water rocky bottoms and coralligenous assemblages, namely Nemertesia antennina, Eudendrium rameum, Filellum serpens, Dynamena disticha, Clytia hemisphaerica, Hebella scandens, Sertularella polyzonias, S. gayi, S. ellisi, S. crassicaulis, Laomedea angulata and Cuspidella humilis. The only detailed study of hydrozoans found on coralligenous assemblages is that of Llobet et al. (1991a), who report 35 species of hydroids living on the thalli of Halimeda tuna in the coralligenous concretions of Tossa de Mar (northwestern Mediterranean). Llobet et al. (1991a) 150

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classify the most abundant hydrozoans into three categories on the basis of their horizontal zonation on the thalli. The hydroids common on the proximal articles (oldest) are relatively large and present throughout the year (Eudendrium racemosum, E. capillare, Halecium tenellum and Kirchenpaueria echinulata). Those common on the medial articles (Campalecium medusiferum, Halecium pusillum, Hydranthea margarica, Phialella quadrata, Campanularia everta and Filellum serpens) are smaller and often occur in dense monospecific patches. Finally, those common on the distal articles (Campanularia raridentata, Clytia hemisphaerica, Sertularia distans, Sertularella polyzonias and Aglaophenia pluma) are present for only short periods and are highly opportunistic. This zonation seems to reflect interspecific niche selection, enabling successful competition for space with other hydroids, algae and bryozoans. Anthozoa Studies by Laubier (1966), True (1970), Hong (1980) and Gili et al. (1984, 1989) report several species of anthozoans from coralligenous habitats (up to 33 in Gili et al. 1984). The commonest species are Parazoanthus axinellae, Leptopsammia pruvoti, Parerythropodium coralloides, Alcyonium acaule, Paramuricea clavata, Eunicella singularis, E. cavolinii, Rolandia rosea, Corallium rubrum, Telmatactis elongata, Maasella edwardsii, Monomyces pygmaea, Hoplangia durotrix, Caryophyllia inornata, C. smithii, Clavularia ochracea, Cornularia cornucopiae and Epizoanthus arenaceus. Madracis pharensis is especially abundant in the coralligenous outcrops of the eastern Mediterranean (Laborel 1960). Scyphozoa The only species reported (Hong, 1980) is Nausitoë punctata, living inside several massive sponges. Turbellaria Laubier (1966) reports three turbellarians from the coralligenous communities of Banyuls, all very rare. Nemertea Nemerteans live endolithically in concretions. According to Pruvot (1897) and Laubier (1966), who report up to 12 species in the coralligenous communities of Banyuls, they are rather common. Drepanophorus crassus, Tetrastemma coronatum, Micrura aurantiaca and M. fasciolata are the most abundant. Nematoda Nematodes are the most abundant microscopic metazoans in marine sediments and are present in the sediments retained in coralligenous assemblages, as well as in the endofauna of concretions and the epifauna of algae and sessile invertebrates. However, there are no studies dealing with this group of organisms in coralligenous assemblages. Polychaeta Polychaetes are extremely abundant in coralligenous communities. Martin (1987) reported a total of 9195 individuals present in 20 samples of 400 cm2 collected from coralligenous communities dominated by Mesophyllum alternans and Lithophyllum frondosum from the Catalan coast (northwestern Mediterranean). This means an average of 460 worms per sample and a density of more than one individual per cm2. He found 191 species, with a dominance of Syllidae (31% of the total). The number of species per sample was very high, ranging between 32 and 71 for macrofauna 151

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(>0.4 mm) and between 27 and 55 for microfauna (70%) remained almost constant throughout the 2 yr of monitoring, showing no or few transitions, and this indicates the great persistence of the animals and plants that thrive in coralligenous communities (Figure 18). Other studies have been conducted with some components or species of coralligenous communities. In fact, most studies dealing with the biology of the main species in coralligenous communities (see next section) have described the effects of seasonality, when this process exists. In terms of benthic flora, Ballesteros (1991a) described the seasonal cycle of several phytobenthic communities from the northwestern Mediterranean, making a between-community comparison using the same variables as descriptors. The coralligenous community with Mesophyllum alternans and Halimeda tuna had the lowest seasonality of all the subtidal communities studied, this being almost constant in autumn, winter and spring, but with peak productivity in summer, 165

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Figure 18 (See also Colour Figure 18 in the insert.) Maps of transition intensity resulting from overlay procedures of images from the same plot (310 cm2) along a depth gradient in a vertical wall at the Medes Islands (NE Spain) during 2 yr of sampling. Patch colour denotes number of changes taking place in each patch (see legend). Coralligenous communities (14 and 20 m depth) display much lower transition rates than shallow water communities, indicating high persistence and low rates of change in the animals and plants thriving in the coralligenous communities. (From Garrabou et al. 2002. With permission from Elsevier.)

during which time there were higher biomass values than for the rest of the year. Piazzi et al. (2004) found significant seasonal differences that were mostly related to the disappearance of many turf species and the decrease in cover of most erect algae, principally foliose and corticated-terete forms, in winter. Although growth of coralline algae is almost constant throughout the year (Garrabou & Ballesteros 2000), Halimeda growth occurs mainly in summer (Ballesteros 1991c). In terms of structural changes in the community, two stages can be discerned over an annual cycle: a diversified community stage, with a reduced coverage of Halimeda and other soft algae, and a developed community stage, characterized by a high coverage of Halimeda (Ballesteros 1991b). The shift from the diversified community stage to the developed community stage takes place through a production phase (early summer). A diversification phase can be distinguished in late autumn, when a sudden fall in Halimeda coverage is detected (Ballesteros 1991b) (Figure 19). Most benthic hydrozoans exhibit a seasonal pattern, with reproduction in spring or autumn and growth from autumn to spring; most of them disappear during the summer, leaving only dormant basal stolons (Boero et al. 1986). Epiphytic hydrozoans on Halimeda tuna decline in abundance in summer because of the death of old thalli of Halimeda, the growth of new thalli and apical articles on existing thalli, and possibly because of interspecific competition with epiphytic algae (Llobet et al. 1991a). 166

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Production phase

SUMMER

Developed community

AUTUMN

SPRING

Diversified community

WINTER

Diversification phase

Figure 19 Although seasonality in structural patterns is not very evident in coralligenous communities, assemblages of the green alga Halimeda tuna show high production in summer, higher biomass in autumn, low production in winter and high spatial heterogeneity in spring, going through the two stages of a diversified community (spring) and a developed community (autumn). (From Ballesteros 1991a.)

Anthozoans exhibit a marked seasonality in all activities (Coma et al. 1998a, Garrabou 1999). According to Coma et al. (2002) respiration rates of Paramuricea clavata, Dysidea avara and Halocynthia papillosa vary two- to three-fold across the annual cycle, exhibiting a marked seasonal pattern but showing no daily cycle or significant day-to-day variability within months. The respiration rate of Paramuricea (a passive suspension feeder) does not correlate with temperature, but that of Dysidea and Halocynthia (active suspension feeders) increases with temperature. There is a low rate of new tissue synthesis during summer, together with the contraction of polyps and a low Q10, which explains the low respiration rates of Paramuricea observed during the period of highest temperature. These low respiration rates support the hypothesis that energy limitations may underlie summer dormancy in some benthic suspension-feeding taxa in the Mediterranean (Figure 20). 22

100 75

18 16

50

14 25 12 10

Activity rhythm (%)

Temperature (°C)

20

0 J F M A M J J A S O N D Time

Figure 20 Activity rhythm in the gorgonian Paramuricea clavata, estimated as a percentage of expanded colonies, displays a strong decrease in summer, in conjunction with high water temperatures. This, and other evidence of decreased activity (i.e., growth and reproduction), in Paramuricea, as well as in other suspensionfeeders, prompted Coma et al. (2002) to describe summer dormancy for many Mediterranean benthic invertebrates. (From Coma et al. 1998a. With permission from Inter-Research.)

167

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There is growing evidence that seasonal patterns of activity and secondary production of suspension feeders in coralligenous assemblages are characterized by aestivation (Coma et al. 2000). Several types of resting and resistance periods have been observed in several colonial ascidians in the warm season (Turon 1992, Turon & Becerro 1992). In the case of Polysyncraton lacazei the surface of the colonies is covered by a glassy pellicle and the siphonal apertures are sealed. This state is interpreted as a rejuvenative phenomenon that extends the life span of the zooids (Turon 1992). Some sponges also go through a resting, nonfeeding period with cellular restructuring, mainly in summer. For example, some specimens of Crambe crambe appear to be covered by a glassy cuticle, obliterating the oscula and ostia after reproduction, from the end of August until the end of October (Turon et al. 1999). These authors suggest that these resting stages develop not only in response to remodelling following reproduction, but also as an effect of water temperature abnormalities. The decapod fauna also displays a certain seasonality (García-Raso & Fernández Muñoz 1987), due to the intense recruitment of several species in late summer, and a progressive decrease in the density of individuals and an increase in their size from October to June. The fish fauna of coralligenous communities is also affected by seasonality (Garcia-Rubies 1997), although its effect is of very minor importance. The number of species in fish counts along 50 m-long visual transects of the coralligenous bottoms around the Medes Islands slightly decreases in winter, and most fishes seem to be less active than in summer.

Functioning of outstanding and key species Several studies of coralligenous concretions are devoted to species that are particularly abundant, are architecturally important or are economically valuable. A compilation of the major knowledge of these species is presented here.

Coralline algae Growth dynamics of two important coralligenous builders in the northwestern Mediterranean, Mesophyllum alternans and Lithophyllum frondosum, were studied in the bioconcretions of the Medes Islands marine reserve, in a steep wall situated at a depth of between 15 and 30 m (Garrabou & Ballesteros 2000). Growth rates ranged from 0.16 month–1 for Mesophyllum alternans to 0.09 month–1 for Lithophyllum frondosum, with shrinkage rates being 0.09 and 0.04 month–1, respectively. These growth rates are more than one order of magnitude lower than those reported for other Mediterranean and tropical coralline species, but similar to reports for crustose corallines in Arctic and temperate waters. No seasonal pattern in growth or shrinkage was found for either species, although seasonality in conceptacle occurrence was detected in Lithophyllum frondosum, with a high interannual variability. Mesophyllum alternans thalli frequently underwent fissions and fusions (almost one event during the 2-yr monitoring period for 50% of monitored plants), while they were rarely observed in Lithophyllum frondosum. These differences in growth, shrinkage, and fission and fusion events are interpreted as different growth strategies. Mesophyllum alternans has a more opportunistic strategy, growing faster and gaining area more rapidly, although it also loses area at higher rates. Lithophyllum frondosum has a more conservative strategy and is more effective in maintaining the area acquired through its reduced growth rate (Garrabou & Ballesteros 2000).

Halimeda tuna Growth and production of a Halimeda tuna population from a coralligenous community (18 m depth) in the northwestern Mediterranean was studied by Ballesteros (1991c). The production of new segments changed seasonally, being maximal in summer and minimal in winter (Figure 21), 168

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800 production loss

700

Segments

600 500 400 300 200 100 0 J-F

M-A

M-J J-A Time

S-O

N-D

Figure 21 Seasonal changes in segment production and loss for a population of the green alga Halimeda tuna at 18 m depth in a coralligenous wall off Tossa de Mar (NE Spain). (From Ballesteros 1991c. With permission from Walter de Gruyter GmbH & Co. KG.)

and this suggests that growth is mainly related to temperature and irradiance. The loss of segments seemed to be related to physical disturbances (storms) and herbivory. Annual production of H. tuna was estimated at 680 g dw m–2, equivalent to 114 g organic C m–2 yr–1 and to 314 g CaCO3 m–2 yr–1; the yearly P/B ratio was 1.87 yr–1. The epiphytic assemblage growing on the segments of H. tuna also displayed high seasonality, with a maximum biomass and species richness in early summer. Values of growth and production reported in Ballesteros (1991c) emphasize the importance of H. tuna as a producer both of organic matter and calcium carbonate in the coralligenous habitat. In fact, available data suggest that calcium carbonate production by Halimeda in shallow coralligenous concretions is similar to that of coralline algae (Canals et al. 1988).

Porifera Garrabou & Zabala (2001) studied the growth dynamics of four demosponges (Crambe crambe and Hemimycale columella from a ‘precoralligenous’ community, and Oscarella lobularis and Chondrosia reniformis from a coralligenous community in the Medes Islands), and reported relatively slow growth dynamics with low growth and shrinkage rates. The coralligenous species had an average relative growth rate of 0.15 month–1 (Oscarella) and 0.022 month–1 (Chondrosia), with shrinkage rates of 0.12 and 0.017 month–1, respectively. Interspecific differences in growth, shrinkage, division and fusion rates were interpreted as evidence of distinct biological strategies aimed at persistence and the occupation of substratum. Chondrosia reniformis is conservative, with slow growth but great resistance to damage. Crambe crambe seems to enhance its rate of space occupation by a high division rate. Hemimycale columella grows quickly and shrinks at low rates, thus spreading rapidly over the substratum. Oscarella lobularis grows and shrinks rapidly, showing great overall growth. Dysidea avara, a common sponge in coralligenous communities (Uriz et al. 1992a) obtained 85% of its ingested carbon from the fraction 5 µm (mostly phytoplankton) (Ribes et al. 1999b). However, the partial contributions of the different groups varied seasonally, in accordance with the planktonic composition of the water column. During winter, phytoplankton was an important component of the total uptake (26%), whereas during the rest of the year it contributed 1 polychaete worm cm–2. Some endangered Mediterranean species live in the coralligenous habitat, although none is exclusive to this environment. As its diversity is so great, the coralligenous habitat reveals an intense connectivity among its inhabitants. Space competition is strong because the space is completely saturated by organisms, and epibiosis is extremely frequent. Alellochemicals must play an important role in space competition 179

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because coralligenous communities exhibit a very high percentage of chemically active species. Trophic relationships are also strong in coralligenous communities, particularly among vagile species because most of the sessile invertebrates have skeletons that deter feeding. Several examples of mutualism, commensalism and parasitism have been reported. Growth of coralligenous accretions, carbonate production, and bioerosion and sedimentation rates have merited very few studies, although those published have presented very valuable data. They indicate (1) very low accumulation rates which are related to water depth and light availability; (2) the important source of carbonate for the continental shelf represented by coralligenous buildups; (3) relatively low bioerosion rates, at least in deep waters where algal growth is the lowest; and (4) relatively high sedimentation rates. Accretion rates of up to 0.83 mm yr–1, carbonate production (vegetal and animal) of up to 1000 g CaCO3 m–2 yr–1, and values for bioerosion of up to 220 g CaCO3 m–2 year–1 have been reported. These values are always higher in shallow than in deep waters. Large animals and plants of coralligenous assemblages are highly persistent, and show low to nil seasonality in terms of space occupation. Most of the area covered by a coralligenous community remains unchanged after, for example, 2 yr of monitoring. However, growth pulses have been detected in some organisms such as the green alga Halimeda tuna or its epiphytic hydrozoans. Vagile invertebrates and the fish fauna also show a degree of seasonality, mainly due to recruitment pulses and inactivity in winter. Several suspension feeders also exhibit some physiological seasonality, with decreased activity in summer, probably related to the low food availability and high temperatures that occur during this season. Some species inhabiting coralligenous assemblages (algae Mesophyllum alternans, Lithophyllum frondosum and Halimeda tuna; sponges Hemimycale columella, Crambe crambe, Chondrosia reniformis, Dysidea avara and Oscarella lobularis; hydrozoans Orthopyxis crenata, Halecium petrosum and H. pusillum; anthozoans Paramuricea clavata, Eunicella cavolinii, E. singularis, Corallium rubrum, Alcyonium acaule, Parazoanthus axinellae; tunicates Halocynthia papillosa, Cystodytes dellechiajei and Microcosmus sabatieri) have been carefully studied in order to determine one or several of the following features: growth rates, population dynamics, age, carbonate production, natural diets, prey capture, reproduction, spawning and recruitment patterns. Five main causes of disturbance that affect coralligenous assemblages have been distinguished: 1. Large-scale events, involving mass mortalities of suspension feeders, seem to be related to summer high water column stability and high temperatures but their ultimate causes remain unclear. It has been suggested that they are related to the current global warming trend. 2. Waste waters profoundly affect the structure of coralligenous communities by inhibiting coralline algal growth, increasing bioerosion rates, decreasing species richness and densities of the largest individuals of the epifauna, eliminating some taxonomical groups (e.g., most echinoderms, bryozoans and crustaceans), and increasing the abundance of highly tolerant species. 3. Fishing is another cause of coralligenous degradation. Trawling is especially destructive, for not only does it physically destroy the coralligenous structure but it also increases turbidity and sedimentation rates, which negatively affects algal growth and suspension feeding. Traditional, as well as recreational, fishing mainly affect target species, although most of them rapidly recover after fishing prohibition or after implementation of scientifically guided fisheries management. However, this is not the case for the long-lived and slow-growing red coral, whose full recovery from harvesting has been estimated to take several decades or even centuries.

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4. Diver activity is another cause of recent degradation of coralligenous assemblages, although this kind of disturbance only affects, at the moment, very few areas situated at the most popular sites for recreational diving. 5. Finally, invasive alien species are another cause of concern because their numbers are increasing throughout the Mediterranean. Especially dangerous for the coralligenous communities is the red turf alga Womersleyella setacea, which forms a dense carpet over encrusting corallines, thus inhibiting photosynthesis and growth of the main coralligenous builders.

Actions Gaps in scientific knowledge In terms of the current state of scientific knowledge of the coralligenous habitat it is easy to detect several gaps that make it rather difficult to make recommendations for protecting coralligenous assemblages: 1. There is a complete lack of knowledge of the distribution of coralligenous substrata in the Mediterranean, with the exception of some extremely limited areas situated mainly in marine parks or reserves. As a minimum, approximate cartography and quantification of these bottoms is required. 2. It is highly recommended that a list of all the organisms that have been found living in coralligenous communities be drawn up, in order to have a precise idea of the amount of biodiversity contained in this environment. 3. Almost nothing is known about the coralligenous concretions from the eastern Mediterranean. Special efforts must be made to investigate the description and functioning of coralligenous communities in this area. 4. Further studies dealing with the processes involved in the buildup and erosion of coralligenous assemblages must be conducted because almost all the existing information comes from one or two localities situated in the northwestern Mediterranean. 5. An understanding of the functioning of the dominant and keystone species is essential in order to implement an adequate management strategy for the coralligenous habitat. 6. The effect of disturbances in coralligenous assemblages is poorly understood, and there are no data at all on the capacity of this environment to recover (with the exception of fish stocks after fishing prohibition). The following issues would appear to be particularly important: a. Indirect impact of trawling b. Impact of waste-water dumping c. Effects of alien species invasion d. Causes of recent large-scale mortality events

Recommendations for protecting coralligenous communities In the light of current knowledge, there are a number of recommendations that can be made in order to conserve (or even improve) coralligenous environments. Most of these recommendations concern not only the coralligenous habitat but most of the coastal benthic habitats because wastewater dumping, trawling and overfishing, and invasion by alien species are problems that affect the whole of the coastal area. Measures to reduce these impacts may improve the overall quality

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of the marine coastal environment. Specific measures aimed at protecting the coralligenous environment might include the following: 1. Waste-water dumping should be banned over coralligenous bottoms, and in their vicinity. 2. Trawling must be completely prohibited in areas with coralligenous outcrops and their vicinity, the aim being to avoid not only the physical damage caused by trawling over coralligenous assemblages but also the indirect effects due to increased turbidity and silting. 3. Any other anthropogenic activity involving an increase in water turbidity and/or sediment removal (e.g., coastline modification, beach regeneration) should be avoided in the vicinity of coralligenous outcrops. 4. Correct management of traditional and recreational fisheries must be implemented in order to prevent stock depletion of target fish and crustaceans. 5. The impact of diving must be compatible with the normal functioning and conservation of the coralligenous environment. 6. The enactment of suitable legislation concerning the introduction of alien species is urgently needed.

Acknowledgements This review was funded by the GEF Strategic Action Plan for the Conservation of Biological Diversity (SAP BIO) project, supported by the United Nations Environment Programme — Mediterranean Action Plan (UNEP-MAP) under the responsibility of the Regional Activity Centre for Specially Protected Areas (RAC/SPA). I am indebted to Drs Joaquim Garrabou, Rafel Coma, Antoni Garcia-Rubies, Daniel Martin, Enrique Macpherson, María Jesús Uriz, Xavier Turon, Mikel Zabala and Jordi Camp for providing ecological and taxonomical advice and bibliography. Jordi Corbera and Mikel Zabala are kindly acknowledged for providing the artwork. I am also grateful to Dr. Marc Verlaque for his advice on coralline algae nomenclature, and to Dr. Jean Georges Harmelin for providing the picture and data for Figure 22.

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MEDITERRANEAN CORALLIGENOUS ASSEMBLAGES Mayol, J., Grau, A., Riera, F. & Oliver, J. 2000. Llista vermella dels peixos de les Balears. Quaderns de Pesca 4, 1–126. Meinesz, A. 1999. Killer Algae: The True Tale of a Biological Invasion. Chicago & London: University of Chicago. Meinesz, A. & Hesse, B. 1991. Introduction et invasion de l’algue tropicale Caulerpa taxifolia en Méditerranée nord-occidentale. Oceanologica Acta 14, 415–426. Mistri, M. & Ceccherelli, V.U. 1994. Growth and secondary production of the Mediterranean gorgonian Paramuricea clavata. Marine Ecology Progress Series 103, 291–296. Molinier, R. 1956. Les fonds à laminaires du Grand Banc de Centuri (Cap Corse). Comptes Rendus de l’Académie des Sciences 342, 939–941. Molinier, R. 1960. Étude des biocénoses marines du Cap Corse. Vegetatio 9, 212–312. Montserrat, A. 1984. Els equinoderms de les illes Medes. In Els Sistemes Naturals de les Illes Medes, J. Ros et al. (eds), Arxius Secció Ciències 73, 563–580. Munar, J. 1993. Els equinoderms. In Història Natural de l’Arxipèlag de Cabrera, J.A. Alcover et al. (eds), Monografies de la Societat d’Història Natural de Balears 2. Palma de Mallorca: CSIC-Ed. Moll, 597–606. Munilla, T. & De Haro, A. 1984. Picnogònids de les illes Medes. In Els Sistemes Naturals de les Illes Medes, J. Ros et al. (eds), Arxius Secció Ciències 73, 531–536. Nikolic, M. 1960. Hippodiplosia foliacea Solander, 1876 (Bryozoa), comme centre d’association sur un fond coralligène dans l’Adriatique. Rapport et Procès Verbaux des Réunions Commission Internationale pour l’Exploration Scientifique de la Mer Méditerranée 15 (2), 85–86. Odum, H.T. & Odum E.P. 1955. Trophic structure and productivity of a windward coral reef community on Eniwetok Atoll. Ecological Monographs 25, 291–320. Ortiz, A., Massó, C., Soriano, O. & Limia, J. 1986. La barra italiana como arte de pesca del coral rojo (Corallium rubrum L.) en el mar de Alborán (SE de España). Boletín Instituto Español de Oceanografía 3, 83–92. Palanques, A., Guillén, J. & Puig, P. 2001. Impact of bottom trawling on water turbidity and muddy sediment of an unfished continental shelf. Limnology and Oceanography 46, 1100–1110. Parenzan, P. 1960. Aspetti biocenotici dei fondi ad alghe litoproduttrici del Mediterraneo. Rapport et Procès Verbaux des Réunions Commission Internationale pour l’Exploration Scientifique de la Mer Méditerranée 15 (2), 87–107. Pascual, J. & Flos, J. 1984. Metereologia i Oceanografia. In Els Sistemes Naturals de les Illes Medes, J. Ros, I. Olivella & J.M. Gili (eds), Arxius Secció Ciències 73, 75–114. Patzner, R.A. 1998. The invasion of Lophocladia (Rhodomelaceae, Lophotalieae) at the northern coast of Ibiza (Western Mediterranean Sea). Bolletí de la Societat d’Història Natural de les Balears 41, 75–80. Patzner, R.A. 1999. Habitat utilization and depth distribution of small cryptobenthic fishes (Blenniidae, Gobiidae, Trypyterigiidae) in Ibiza (western Mediterranean Sea). Environmental Biology of Fishes 55, 207–214. Pérès, J. 1967. The Mediterranean benthos. Oceanography and Marine Biology: An Annual Review 5, 449–533. Pérès, J. & Picard, J.M. 1951. Notes sur les fonds coralligènes de la région de Marseille. Archives de Zoologie Expérimentale et Générale 88, 24–38. Pérès, J. & Picard, J.M. 1952. Les corniches calcaires d’origine biologique en Méditerranée Occidentale. Recueil des Travaux de la Station Marine d’Endoume 4, 2–33. Pérès, J. & Picard, J.M. 1958 Recherches sur les peuplements benthiques de la Méditerranée nord-orientale. Annales de l’Institut Océanographique de Monaco 34, 213–291. Pérès, J. & Picard, J.M. 1964. Nouveau manuel de bionomie benthique de la mer Méditerranée. Recueil des Travaux de la Station Marine d’Endoume 31(47), 1–131. Perez, T., Garrabou, J., Sartoretto, S., Harmelin, J.G., Francour, P. & Vacelet, J. 2000. Mortalité massive d’invertébrés marins: un événement sans précédent en Méditerranée nord-occidentale. Comptes Rendus de l’Académie des Sciences Série III, Life Sciences 323, 853–865. Piazzi, L., Balata, D., Pertusati, M. & Cinelli, F. 2004. Spatial and temporal variability of Mediterranean macroalgal coralligenous assemblages in relation to habitat and substratum inclination. Botanica Marina 47, 105–115.

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ENRIC BALLESTEROS Piazzi, L., Ceccherelli, G., Meinesz, A., Verlaque, M., Akali, B. Antolic, B., Argyrou, M., Balata, D., Ballesteros, E., Calvo, S., Cinelli, F., D’Archino, R., Djellouli, A.S., Javel, F., Mifsud, C., Pala, D., Panayotidis, P., Peirano, A., Pergent, G., Petrocelli, A., Ruitton, S. & Zuljevic, A. 2005. Invasion of Caulerpa racemosa (Caulerpales, Chlorophyta) in the Mediterranean Sea: the balance of thirteen years of spread. Cryptogamie Algologie 26, 189–202. Piazzi, L., Pardi, G., Balata, D., Cecchi, E. & Cinelli, F. 2002. Seasonal dynamics of a subtidal north-western Mediterranean macroalgal community in relation to depth and substrate inclination. Botanica Marina 45, 243–252. Piazzi, L., Pardi, G. & Cinelli, F. 1996. Ecological aspects and reproductive phenology of Acrothamnion preissii (Sonder) Wollaston (Ceramiaceae, Rhodophyta) from the Tuscan Archipelago (Western Mediterranean). Cryptogamie Algologie 17, 35–43. Pruvot, G. 1894. Sur les fonds sous-marins de la région de Banyuls et du cap de Creus. Comptes Rendus de l’Académie des Sciences 118, 203–206. Pruvot, G. 1895. Coup d’oeil sur la distribution générale des invertébrés dans la région de Banyuls (Golfe du Lion). Archives de Zoologie Expérimentale et Générale 3, 629–658. Pruvot, G. 1897. Essai sur les fonds et la faune de la Manche Occidentale (côtes de Bretagne) comparées à ceux du Golfe de Lion. Archives de Zoologie Expérimentale et Générale 5, 511–660. Ramos, A.A. 1991. Ascidias litorales del Mediterráneo ibérico. Faunística, ecología y biogeografía. Tesis Doctoral. Universidad de Alicante. Ribes, M., Coma, R. & Gili, J.M. 1998. Seasonal variation of in situ feeding rates by the temperate ascidian Halocynthia papillosa. Marine Ecology Progress Series 175, 201–213. Ribes, M., Coma, R. & Gili, J.M. 1999a. Seasonal variation of particulate organic carbon, dissolved organic carbon and the contribution of microbial communities to the live particulate organic carbon in a shallow near-bottom ecosystem at the Northwestern Mediterranean Sea. Journal of Plankton Research 21, 1077–1100. Ribes, M., Coma, R. & Gili, J.M. 1999b. Natural diet and grazing rate of the temperate sponge Dysidea avara (Demospongiae, Dendroceratida) throughout an annual cycle. Marine Ecology Progress Series 176, 179–190. Ribes, M., Coma, R. & Gili, J.M. 1999c. Heterogenous feeding in benthic suspension feeders: the natural diet and grazing rate of the temperate gorgonian Paramuricea clavata (Cnidaria: Octocorallia) over a year cycle. Marine Ecology Progress Series 183, 125–137. Riedl, R. 1966. Biologie der Meereshöhlen. Hamburg: Paul Parey. Riera, F., Oliver, J. & Terrassa, J. 1998. Peixos de les Balears. Palma de Mallorca: Govern Balear. Riera, F., Pou, S. & Grau, A.M. 1993. La ictiofauna. In Història Natural de l’Arxipèlag de Cabrera, J. A. Alcover et al. (eds), Monografies de la Societat d’Història Natural de Balears 2. Palma de Mallorca: CSIC-Ed. Moll, 623–644. Rivoire, G. 1991. Mortalité du corail et des gorgones en profondeur au large des côtes provençales. In Les Espèces Marines à Protéger en Méditérranée, C.F. Boudouresque et al. (eds), Marseille: GIS Posidonie, 53–59. Romano, J.C., Bensoussan, N., Younes, W.A.N. & Arlhac, D. 2000. Anomalies thermiques dans les eaux du Golfe de Marseille durant l’été 1999. Une explication partielle de la mortalité des invertébrés fixés. Comptes Rendus de l’Académie des Sciences Série III, Life Sciences 323, 853–865. Ros, J. 1978. La alimentación y el sustrato en los opistobranquios ibéricos. Oecologia Aquatica 3, 153–166. Ros, J., Olivella, I. & Gili, J.M. (eds). 1984. Els Sistemes Naturals de les Illes Medes. Arxius Secció Ciències 73, Barcelona: Institut d’Estudis Catalans. Ros, J., Romero, J., Ballesteros, E. & Gili, J.M. 1985. Diving in blue water: the benthos. In Western Mediterranean, R. Margalef (ed.), Oxford: Pergamon, 233–295. Rosell, D. & Uriz, M.J. 2002. Excavating and endolithic sponge species (Porifera) from the Mediterranean: species descriptions and identification key. Organisms Diversity and Evolution 2, 55–86. Rosell, D., Uriz, M.J. & Martin, D. 1999. Infestation by excavating sponges on the oyster (Ostrea edulis) populations of the Blanes littoral zone (northwestern Mediterranean Sea). Journal of the Marine Biological Association of the United Kingdom 79, 409–413.

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MEDITERRANEAN CORALLIGENOUS ASSEMBLAGES Rossi, L. 1958. Osservazioni sul bentos coralligeno dei dintorni di Catania. Archivi di Oceanografia e Limnologia 11, 161–165. Rossi, L. 1961. Sur un faciès à gorgonaires de la pointe du Mesco (Golfe de Gènes) (note préliminaire). Rapports et Procés-Verbaux des Réunions Commission Internationale pour l’Exploration Scientifique de la Mer Méditerranée 16 (2), 517–521. Rossi, S. 2001. Environmental factors affecting the trophic ecology of benthic suspension feeders. PhD Thesis. University of Barcelona. Russo, G.F. & Cicogna, F. 1991. The date mussel (Lithophaga lithophaga), a “case” in the Gulf of Naples. In Les Espèces Marines à Protéger en Méditérranée, C.F. Boudouresque et al. (eds), Marseille: GIS Posidonie, 141–150. Rützler, K. 1976. Ecology of Tunisian commercial sponges. Tethys 7, 249–264. Sala, E., Boudouresque, C.F. & Harmelin-Vivien, M. 1998. Fishing, trophic cascades and the structure of algal assemblages: evaluation of an old but untested paradigm. Oikos 82, 425–439. Sala, E., Garrabou, J. & Zabala, M. 1996. Effects of diver frequentation on Mediterranean sublittoral populations of the bryozoan Pentapora fascialis. Marine Biology 126, 451–459. Salas, C. & Hergueta, E. 1986. Fauna de moluscos de las concreciones calcáreas de Mesophyllum lichenoides (Ellis) Lemoine. Estudio de la diversidad de un ciclo anual. Iberus 6, 57–65. Santangelo, G. & Abbiati, M. 2001. Red coral: conservation and management of an over-exploited Mediterranean species. Aquatic Conservation of Marine and Freshwater Ecosystems 11, 253–259. Santangelo, G., Abbiati, M., Giannini, F. & Cicogna, F. 1993. Red coral fishing trends in the western Mediterranean Sea during the period 1981–1991. Scientia Marina 57, 139–143. Santangelo, G., Carletti, E., Maggi, E. & Bramanti, L. 2003. Reproduction and population sexual structure of the overexploited Mediterranean red coral Corallium rubrum. Marine Ecology Progress Series 248, 99–108. Sarà, M. 1968. Un coralligeno di piattaforma (coralligène de plateau) lungo il littorale pugliese. Archivi di Oceanografia e Limnologia 15 (Suppl.), 139–150. Sarà, M. 1969. Research on coralligenous formation: problems and perspectives. Pubblicazioni della Stazione Zoologica di Napoli 37, 124–134. Sartoretto, S. 1994. Structure et dynamique d’un nouveau type de bioconstruction à Mesophyllum lichenoides (Ellis) Lemoine (Corallinales, Rhodophyta). Comptes Rendus de l’Académie des Sciences Série III, Life Sciences 317, 156–160. Sartoretto, S. 1996. Vitesse de croissance et bioérosion des concrétionnements “coralligènes” de Méditerranée nord-occidentale. Rapport avec les variations Holocènes du niveau marin. Thèse Doctorat d’Écologie, Université d’Aix-Marseille, II. Sartoretto, S. 1998. Bioérosion des concrétions coralligènes de Méditerranée par les organismes perforants: essai de quantification des processus. Comptes Rendus de l’Académie des Sciences Séries IIA, Earth and Planetary Sciences 327, 839–844. Sartoretto, S. & Francour, P. 1997. Quantification of bioerosion by Sphaerechinus granularis on “coralligène” concretions of the western Mediterranean. Journal of the Marine Biological Association of the United Kingdom 77, 565–568. Sartoretto, S., Francour, P., Harmelin, J.G. & Charbonnel, E. 1997. Observations in situ de deux Labridae profonds, Lappanella fasciata et Acantholabrus palloni, en Méditerranée nord-occidentale. Cybium 21, 37–44. Sartoretto, S., Verlaque, M. & Laborel, J. 1996. Age of settlement and accumulation rate of submarine “coralligène” (–10 to –60 m) of the northwestern Mediterranean Sea; relation to Holocene rise in sea level. Marine Geology 130, 317–331. Simkiss, K. 1964. Phosphates as crystalpoisons of calcification. Biological Reviews 39, 487–505. Spanier, E. 1991. Artificial reefs to insure protection of the adult Mediterranean slipper lobster, Scyllarides latus. In Les Espèces Marines à Protéger en Méditérranée, C.F. Boudouresque et al. (eds), Marseille: GIS Posidonie, 179–185. Templado, J. 1991. Las especies del género Charonia (Mollusca: Gastropoda) en el Mediterráneo. In Les Espèces Marines à Protéger en Méditérranée, C.F. Boudouresque et al. (eds), Marseille: GIS Posidonie, 133–140.

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ENRIC BALLESTEROS Templado, J., García-Carrascosa, M., Baratech, L., Capaccioni, R., Juan, A., López-Ibor, A., Silvestre, R. & Massó, C. 1986. Estudio preliminar de la fauna asociada a los fondos coralíferos del mar de Alborán (SE de España). Boletín Instituto Español de Oceanografía 3, 93–104. Torrents, O., Garrabou, J., Marschal, C. & Harmelin, J.G. 2005. Age and size at first reproduction in the commercially exploited red coral Corallium rubrum (L.) in the Marseilles area (France, NW Mediterranean). Biological Conservation 121, 391–397. Tortonese, E. 1958. Bionomia marina della regione costiera fra punta della Chiappa e Portofino (Riviera Ligure di Levante). Archivi di Oceanografia e Limnologia 11, 167–210. Tortonese, E. 1965. Fauna d’Italia. Echinodermata. Bologna: Calderini. True, M.A. 1970. Étude quantitative de quatre peuplements sciaphiles sur substrat rocheux dans la région marsellaise. Bulletin de l’Institut Océanographique (Monaco) 69 (1401), 1–48. Turon, X. 1990. Distribution and abundance of ascidians from a locality on the northeast coast of Spain. Pubblicazioni della Stazione Zoologoca di Napoli I: Marine Ecology 11, 291–308. Turon, X. 1992. Periods of non-feeding in Polysyncraton lacazei (Ascidiacea: Didemnidae): a rejuvenative process? Marine Biology 112, 647–655. Turon, X. 1993. Els ascidis: faunística i distribució. In Història Natural de l’Arxipèlag de Cabrera, J. A. Alcover et al. (eds), Monografies de la Societat d’Història Natural de Balears 2. Palma de Mallorca: CSIC-Ed. Moll, 607–621. Turon, X. & Becerro, M. 1992. Growth and survival of several ascidian species from the northwestern Mediterranean. Marine Ecology Progress Series 82, 235–247. Turon, X., Galera, J. & Uriz, M.J. 1997. Clearance rates and aquiferous systems in two sponges with contrasting life-history strategies. Journal of Experimental Zoology 278, 22–36. Turon, X., Uriz, M.J. & Willenz, P. 1999. Cuticular linings and remodelisation processes in Crambe crambe (Demospongiae: Poeciclosclerida). Memoirs of the Queensland Museum 44, 617–625. Uriz, M.J., Martin, D., Turon, X., Ballesteros, E., Hughes, R. & Acebal, C. 1991. An approach to the ecological significance of chemically mediated bioactivity in Mediterranean benthic communities. Marine Ecology Progress Series 70, 175–188. Uriz, M.J., Rosell, D. & Martin, D. 1992a. The sponge population of the Cabrera Archipelago (Balearic islands): characteristics, distribution, and abundance of the most representative species. Pubblicazioni della Stazione Zoologica di Napoli I: Marine Ecology 13, 101–117. Uriz, M.J., Rosell, D. & Maldonado, M. 1992b. Parasitism, commensalism or mutualism? The case of Scyphozoa (Coronatae) and horny sponges. Marine Ecology Progress Series 81, 247–255. Uriz, M.J., Rosell, D. & Martin, D. 1992c. Relationships of biological and taxonomic characteristics to chemically mediated bioactivity in Mediterranean littoral sponges. Marine Biology 113, 287–297. Vadas, R.L. & Steneck, R.S. 1988. Zonation of deep water benthic algae in the Gulf of Maine. Journal of Phycology 24, 338–346. Vaissière, R. 1964. Contribution à l’étude bionomique de la Méditerranée Occidentale (côte du Var et des Alpes-Maritimes, côte occidentale de Corse). Fasc. 1: Generalités. Bulletin de l’Institut Océanographique (Monaco) 63 (1310), 1–12. Vaissière, R. & Fredj, G. 1963. Contribution à l’étude de la faune benthique du plateau continental de l’Algérie. Bulletin de l’Institut Océanographique (Monaco) 60 (1272), 1–83. Velimirov, B. 1975. Wachstum und Altersbestimmung der Gorgonie Eunicella cavolinii. Oecologia 19, 259–272. Vicente, N. & Moreteau, J.C. 1991. Statut de Pinna nobilis L. en Méditerranée (Mollusque Eulamellibranche). In Les Espèces Marines à Protéger en Méditérranée, C.F. Boudouresque et al. (eds), Marseille: GIS Posidonie, 159–168. Vighi, M. 1972. Étude sur la reproduction du Corallium rubrum (L.). Vie et Milieu Sèries A 23, 21–32. Weinbauer, M.G. & Velimirov, B. 1995a. Morphological variations in the Mediterranean sea fan Eunicella cavolini (Coelenterata: Gorgonacea) in relation to exposure, colony size and colony region. Bulletin of Marine Science 56, 283–295. Weinbauer, M.G. & Velimirov, B. 1995b. Biomass and secondary production of the temperate gorgonian coral Eunicella cavolini (Coelenterata, Gorgonacea). Marine Ecology Progress Series 121, 211–216.

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MEDITERRANEAN CORALLIGENOUS ASSEMBLAGES Weinberg, S. 1979. The light-dependent behaviour of planulae larvae of Eunicella singularis and Corallium rubrum and its implication for octocorallian ecology. Bijdragen tot de Dierkunde 49, 16–30. Weinberg, S. 1991. Faut-il protéger les gorgones de Méditerranée? In Les Espèces Marines à Protéger en Méditérranée, C.F. Boudouresque et al. (eds), Marseille: GIS Posidonie, 47–52. Weinberg, S. & Weinberg, F. 1979. The life cycle of a gorgonian: Eunicella singularis (Esper, 1794). Bijdragen tot de Dierkunde 48, 127–140. Whitehead, P.J.P., Bauchot, M.L., Hureau, J.C., Nielsen, J. & Tortonese, E. (eds). 1984–1986. Fishes of the North-Eastern Atlantic and the Mediterranean. Vols. I–III. Bungay: Chaucer. Woelkerling, W.J. 1983. A taxonomic reassessment of Lithophyllum (Corallinaceae, Rhodophyta) based on studies of R.A. Philippi’s original collections. British Phycological Journal 18, 299–328. Woelkerling, W.J., Penrose, D. & Chamberlain, Y.M. 1993. A reassessment of type collections of nongeniculate Corallinaceae (Corallinales, Rhodophyta) described by C. Montagne and L. Dufour, and of Melobesia brassica-florida Harvey. Phycologia 32, 323–331. Wray, J.L. 1977. Calcareous Algae. Amsterdam: Elsevier. Zabala, M. 1984. Briozous de les illes Medes. In Els Sistemes Naturals de les Illes Medes, J. Ros et al. (eds), Arxius Secció Ciències 73, 537–562. Zabala, M. 1986. Fauna dels briozous dels Països Catalans. Arxius Secció Ciències 84, 1–833. Zabala, M. & Ballesteros, E. 1989. Surface-dependent strategies and energy flux in benthic marine communities or, why corals do not exist in the Mediterranean. Scientia Marina 53, 3–17. Zabala, M., Garcia-Rubies, A., Louisy, P. & Sala, E. 1997a. Spawning behaviour of the Mediterranean dusky grouper Epinephelus marginatus (Lowe, 1834) (Pisces, Serranidae) in the Medes islands Marine Reserve (NW Mediterranean, Spain). Scientia Marina 61, 65–77. Zabala, M., Louisy, P., Garcia-Rubies, A. & Gracia, V. 1997b. Socio-behavioural context of reproduction in the Mediterranean dusky grouper Epinephelus marginatus (Lowe, 1834) (Pisces, Serranidae) in the Medes islands Marine Reserve (NW Mediterranean, Spain). Scientia Marina 61, 79–89. Zibrowius, H., Monteiro-Marques, V. & Grashoff, M. 1984. La répartition du Corallium rubrum dans l’Atlantique (Cnidaria, Anthozoa: Gorgonaria). Téthys 11, 163–170.

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Oceanography and Marine Biology: An Annual Review, 2006, 44, 197-276 © R. N. Gibson, R. J. A. Atkinson, and J. D. M. Gordon, Editors Taylor & Francis

DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS — FROM HISTOLOGY TO ECOLOGY HEIKE WÄGELE1, MANUEL BALLESTEROS2 & CONXITA AVILA3 1Rheinische Friedrich-Wilhelms-Universität, Institut für Evolutionsbiologie, An der Immenburg 1, 53121 Bonn, Germany and Zoologisches Forschungsmuseum Koenig, Adenauer Allee 160, 53113 Bonn, Germany E-mail: [email protected] 2Facultat de Biologia, Universitat de Barcelona, Av. Diagonal 645, 08028 Barcelona, Catalunya, Spain E-mail: [email protected] 3CEAB-CSIC, c/Accés a la Cala Sant Francesc 14, 17300 Blanes, Girona, Catalunya, Spain E-mail: [email protected]

Abstract Opisthobranch molluscs are an extremely interesting group of animals, displaying a wide diversity in shape, colour and life strategies. Chemical ecology of this group is particularly appealing since most species have a reduced or absent shell and have developed chemical defences to avoid predation. New results on defensive glandular structures as well as a compilation of literature data in sea slugs (Opisthobranchia, Gastropoda, Mollusca) are presented in this review. Investigation of these structures is based on detailed analyses of the histology of many representative species of all major taxa of the Opisthobranchia. The results are correlated with previous and new findings of secondary metabolites in these animals and are set in a phylogenetic context. Additionally, information on food sources is given. Also, an hypothetical scenario relating chemical ecology to histology is proposed. This information will help future analyses to investigate defensive devices on a much more accurate basis and allow a better understanding of evolutionary processes, which are observed independently in many opisthobranch clades.

Introduction Defensive strategies are manifold in Opisthobranchia and comprise cryptic appearance (Edmunds 1987, Wägele & Klussmann-Kolb 2005), formation of spicules (Cattaneo-Vietti et al. 1993, 1995), uptake of nematocysts from cnidarian prey (most recent literature: Gosliner 1994a, Martin & Walther 2002, 2003, Wägele 2004), incorporation of toxic metabolites from the prey, or even de novo synthesis of chemicals. Several reviews have covered the last topic of chemical ecology in molluscs (Karuso 1987, Cimino & Sodano 1989, Faulkner 1988, 1992, 2000, 2001, Pawlik 1993, Avila 1995, 2006, Cimino & Ghiselin 1998, Cimino et al. 2000, Stachowicz 2001, Amsler et al. 2001). Furthermore, some reviews have dealt with natural products from particular groups, such as porostome nudibranchs (Gavagnin et al. 2001), dorids and sacoglossans (Cimino et al. 1999, Cimino & Ghiselin 1998, 1999), or gastropods in general (Cimino & Ghiselin 2001), incorporating 197

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an evolutionary perspective in their analysis. In opisthobranchs, Faulkner & Ghiselin (1983) discussed the importance of the acquisition of defensive chemicals during slug evolution, thus allowing the reduction of the shell (see also Wägele & Klussmann-Kolb 2005). This may have many ecological implications, such as the advantage of searching for new food sources, the exploitation of new habitats, and the development of mantle glands or structures, among others. Cimino & Ghiselin (1999) went even further in claiming that chemical defence is the driving force of opisthobranch evolution. Chemical defence is the main topic in molluscan chemical ecology, although it is by no means the only one. The importance of correctly demonstrating in situ activity against co-occurring predators has been a subject of repeated debate (Faulkner 1992, Avila 1995). However, many compounds are still assumed to have a defensive role without the supporting evidence of reliable ecological experiments. Ecological activity of the compounds has been evaluated in situ, against co-occurring predators for only a few species (Thompson 1960, Avila & Paul 1997, Johnson & Willows 1999, Marín et al. 1999, Avila et al. 2000, Becerro et al. 2001, Gosliner 2001, Iken et al. 2002, Rogers et al. 2002, Penney 2004). The methodological difficulties in carrying out in situ experiments or using co-occuring predators are probably responsible for the scarce information available. To overcome these problems, some studies used predators that do not occur in the same habitat (e.g., Mollo et al. 2005). On the other hand, there is also some literature that deals with parasites on opisthobranchs (Edmunds 1964; Arnaud 1978; Carefoot 1987; Huys 2001; Schrödl 2002, 2003; see also Rudman 2000a) but nothing is known about possible defensive strategies against these parasites. Since the review of the natural products of opisthobranch molluscs published 10 years ago (Avila 1995), many other articles have appeared that deal with opisthobranchs and which describe new interesting aspects of their chemistry (see Faulkner 2002 and previous reports; Blunt et al. 2005). Unfortunately, they cannot all be reviewed here. The geographic variation of natural products in Asteronotus cespitosus (Fahey & Garson 2002) and in Cadlina luteomarginata (Kubanek et al. 2000) has provided new insights into the field. Kubanek et al. (2000) suggested that in some nudibranchs, de novo biosynthesis may be modulated by habitat-specific external factors, thus working only when dietary compounds are not available. The authors suggested this represents an intermediate stage in the evolution of nudibranch chemical defences, between the probably primitive chemical sequestration from diet and the more evolved processes of de novo biosynthesis. The fact that some nudibranchs may only biosynthesise when dietary compounds are not available is an open question that needs to be tested in other species. Among nudibranchs, only C. luteomarginata and Dendrodoris grandiflora seem to possess both dietary sequestered compounds and biosynthetic chemicals (Cimino et al. 1985a, Avila et al. 1991a, Kubanek et al. 2000). Regarding the origin of these compounds, the number of biosynthetic compounds, compared with those obtained from the diet, continues to increase (Garson 1993, Cimino & Sodano 1994, Avila 1995, Faulkner 2002). The sesquiterpene aldehydes of the nudibranch Acanthodoris nanaimoensis are another example of de novo biosynthesis (Graziani & Andersen, 1996). Further studies on biosynthesis include Fontana et al. (1999a, 2003) and Jansen & de Groot (2004), and others reviewed by Garson (2001) and Cimino et al. (2004). Dietary chemicals are selected by a still unknown mechanism. Faulkner (1992) proposed two different mechanisms by which the selection of chemicals could be achieved, but this was never studied in detail. The sea hare Stylocheilus striatus accumulates very different metabolites when offered artificial diets (Pennings & Paul 1993). Fontana et al. (1994b) showed that in the laboratory a chromodoridid species was able to accumulate in the mantle glands compounds from a sponge that is not usually its prey in the field. These experiments would support the idea that the initial role of accumulation structures was that of excretion or autoprotection from the dietary chemicals and evolved later into a defensive mechanism. 198

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DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS

The available information on location and structure of the possible storage organs for chemical defences is scarce and mainly based on literature from the nineteenth to the early twentieth centuries (e.g., Blochmann 1883, Vayssière 1885, Perrier & Fischer 1911). The older literature was reviewed by Hoffmann (1939). More recent studies including histological structures are found, for example, in Edmunds (1966a,b), Thompson & Colman (1984), Thompson (1986), Gosliner (1994a), Wägele (1997), Kolb (1998), Brodie (2005) and Wägele & Klussmann-Kolb (2005). The couple Evelyn and Ernst Marcus, to whom we owe many thorough descriptions of opisthobranchs, very often included histological investigations when describing species, but only in very few cases do these cover defensive glands (also called repugnatorial glands) and then only in a rather sketchy way (e.g., Marcus & Marcus 1955; Marcus 1957, 1958, 1959). The same holds true for many descriptions from the Danish opisthobranch scientist Rudolph Bergh, which are not included here for the same reason. Recent and more extensive investigations on defensive glands are mainly confined to the mantle dermal formations (MDFs) in the doridoidean family Chromodorididae (García-Gomez et al. 1990, 1991; Cimino et al. 1993a; Avila & Paul 1997) and the glands of sea hares (Johnson & Willows 1999). Few investigations deal with epithelial structures or other glandular structures (e.g., Marín et al. 1991, Avila & Durfort 1996, Wägele 1997, Wägele & Klussmann-Kolb 2005). MDFs are suspected to store biochemicals from sponges, the food items of chromodorids. They are discussed as important key characters in the evolution of this particular family (Gosliner & Johnson 1994, Gosliner 2001, Wägele 2004) but, in fact, it is now known that other groups of opisthobranchs that do not forage on sponges also possess MDFs (see Wägele 1997, 2004 and this study). Finding MDFs in a bryozoan-consuming nudibranch (Limacia clavigera) (Wägele 1997) and in an algaeconsuming sacoglossan (Plakobranchus ocellatus (see Wägele 2004)) renders invalid all the previous assumptions of the mantle glands as an exclusive characteristic of the Chromodorididae. Until now, very few attempts have been made to relate knowledge on defensive chemicals to glandular structures known from histology (e.g., Marín et al. 1991 for Tethys fimbria, Marín et al. 1999 for Cephalaspidea). Avila (1993), Fontana et al. (1994b) and Avila & Durfort (1996) showed a preliminary relationship between some defensive glands and natural products for several species of nudibranchs. Actually, all the assumptions on location of chemicals are based on dissection and separation of body parts (e.g., MDFs, mantle border, etc.), and not on cytology or cytochemistry. This is the case in most of the located compounds, such as furanosesquiterpenes of Hypselodoris and Ceratosoma species, diterpenes of Chromodoris species, sesterterpenes of Glossodoris species, or sesquiterpenes of Dendrodorididae. This study tries to fill the gap in the knowledge of the relationship between glandular structures and defensive compounds by summarising histological studies on defensive glands or structures within Opisthobranchia and by tabulating published results on their secondary metabolites. Furthermore, the development of defensive glands, which are supposed to accumulate dietary chemicals in juvenile specimens of Hypselodoris species, was studied in order to ascertain their ontogeny.

Material and methods To analyse the maximum information available on the defensive glands at histological, ecological and chemical levels, several species were selected from each group. Selection was based mainly on the availability of biological material for carrying out rigorous histological studies and also on existing data on ecology and chemistry for the species. However, this proved to be very difficult because very often data are incomplete. For example, data may be available on the chemistry but not on the histology and ecology of a species, and vice versa. Considerable effort has been made to include as many species as possible in the review so that it offers all the information available

199

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in the literature until June 2005. To reduce ambiguity, the taxonomic authorities of all species mentioned in the text are listed in Table 2. For histological analyses, many species were sampled during various expeditions all over the world in recent years, preserved in 4–6% formaldehyde/sea water and stored in 70% ethanol. After dehydration, the specimens were embedded in hydroxyethylmethacrylat (technique developed by Kulzer) (see Wägele 1997). Serial sections (2.5 µm) were stained with Toluidine blue, which specifically stains acid mucopolysaccharides red to violet, and neutral mucopolysaccharides blue. Some of the species investigated were very large and only smaller pieces could be studied histologically. However, this does not allow descriptions to be given of the wider occurrence of the glands, which have a very restricted distribution in the body. For comparison, a few basal pulmonate species are included. For analysis of the chemical composition of some structures (especially the mantle dermal formations), specimens of six species were embedded in Paraplast and sectioned (thickness of sections 5–6 µm). Different staining techniques were applied including two trichrome stains (Poinceau-Acidfuchsin-Azophloxin after Goldner, and Azocarmine-Aniline-Orange G after Heidenhain) and a special staining technique for connective tissue (after Pasini). All methods are described in Böck (1989). Except where noted otherwise, staining records in the text and tables usually refer to Toluidine blue. Hypselodoris villafranca specimens for the ontogenetic studies were collected in Blanes and Tossa (Catalonia, Spain) in August 2003. Sizes of the juveniles ranged from 3–6 mm length. Some adults (15 mm) were also collected and studied to compare with the juveniles of the same populations. They were fixed as described above.

Results Description of glands Nearly all opisthobranch and pulmonate species investigated have more glands than just the repugnatorial or defensive glands and the foot in particular is highly glandular. These latter structures, and others which are more likely involved in crawling (e.g., the tubular foot gland in pulmonates and some cephalaspideans), are not listed here, only those which might be of defensive value. The glandular structures can usually be assigned to certain types, some of which are already well known, others are newly described here. Defensive glandular structures are located in different areas of the animals. They can be located in the epidermis and are therefore part of the outer epidermis. They can lie subepidermally in the notum as single glandular structures or form distinct organs. Some lie in the notum, usually forming rather large organs. In a few cases, large glands are present in the visceral cavity. Table 1 and Figure 1 to Figure 9 give an overview of the types. Table 2 lists all the species investigated during the study and lists some types of glands found in particular species. The food and the chemical structure of the known secondary metabolites from the slug are also provided (Table 2). The glands are described and listed with regard to their location in the organism. Epidermal glandular structures, subepithelial glands, glands in the notum tissue and glands in the visceral cavity are distinguished (see Table 1). Glandular structures confined to the epidermis (Table 1, Table 2 Column 9) Single glandular cells (Table 1) Single glandular cells are mainly located in the notum epithelium and are widely spread. The contents of the vacuoles of the cells mainly stain dark violet, indicating acid mucopolysaccharides. Although morphological and histological complexity is rather low in these 200

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DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS

Table 1 Overview of the different types of glandular structures arranged according to location, composition and staining properties Staining properties Violet staining — indicating acid mucopolysacharides

Bluish staining indicating neutral mucopolysaccharides

Nonstaining — indicating acidic or other substances

Single gland cells in epidermis

Cup cells (e.g., in many Dendronotoidea) (Figure 1A,B)

Cells with a huge vacuole, contents staining homogeneously (Dendrodorididae) (Figure 1B)

Spongy glands (Figure 1C)

Single glands forming a layer

Hypobranchial gland (Figure 1D)

Subepithelial glands

Single glandular cells of moderate size usually opening to the outside (Figure 4B at bottom)

‘Cellules spéciales’ (Figure 1F,G)

Subepithelial acid glands (Pleurobranchoidea) (Figure 2G)

Gland type

Bohadsch gland or opaline gland (Figure 2D,E)

Glandular organs lying in notum

Marginal sacs of Arminidae (Figure 4A)

Blochmann’s glands: some Cephalaspidea (Figure 2A,B) and Anaspidea (here known as ink gland or purple gland) (Figure 2C) Dorsal notum gland (Tylodinoidea) (Figure 3A–C) Interpallial gland (Scaphander) (Figure 3D,E) MDFs (Newnesia, Plakobranchus) (Figure 6A, 7F)

Agglomeration of glandular cells (Thecacera, Cadlina) (Figure 4B,C) MDFs (Chromodorididae) (Figure 5A–F, Figure 6E–G, Figure 7A–F)

MDF-like structures (Doriopsilla, Melibe, etc.) (Figure 6B–D, Figure 9A–F) Complex glands lying inside the body

Median buccal gland (Bourne’s gland) (Pleurobranchoidea, Plocamopherus) (Figure 4D–F)

kinds of cells, a typical appearance of single glandular cells was noticed in many representatives of the Dendronotoidea (Figure 1A, Marionia blainvillea; see also Table 2 Column 9). Here the cuplike glandular cells are characterised by a huge vacuole, staining homogenously dark violet, indicating acid mucopolysaccharides. In other taxa, the contents of the vacuoles may be granular or even homogenous (Figure 1B, Dendrodoris nigra, arrow). This indicates the presence of different substances in the glandular cells. In Roboastra gracilis the glandular epithelium is characterised by numerous extremely tall violet-stained mucous cells with a granular appearance. (continued on page 227) 201

Higher taxon

202

CEPHALASPIDEA Aglajidae

Hydatinidae

+

+

+

Chelidonura pallida Risbec, 1951

Chelidonura tsurugensis Baba & Abe, 1959 ?

+

+

+

+

Hydatina physis Linneus, 1758

+

Chelidonura inornata Baba, 1949

+

+

+

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

3 Hypobranchial gland

0

4 Spongy mantel glands 0

5

Blochmann

+

6

Glandular stripe

+

8

7

MDF TYPE

Pupa solidula Linneus, 1758

Acteon tornatilis Linneus, 1758

Genus and species, authorities

ACTEONOIDEA Acteonidae

2

Column 1 MDF-like structures Special defensive glands

9

Turbellaria (Rudman Web site Seaslugforum) Congeners feed on polychaetes and turbellarians (Burn & Thompson 1998) Congeners feed on polychaetes and turbellarians (Burn & Thompson 1998)

Polychaeta (Rudman Web site Seaslugforum) Polychaeta (Rudman Web site Seaslugforum)

Polychaeta (Rudman Web site Seaslugforum)

Food (references)

10

Unknown

Unknown

Unknown **

Unknown

Unknown

Unknown

Natural products (references)

11

Table 2 Compilation of available data on glandular structures, food and natural products. See notes on page 226.

Wägele & Klussmann-Kolb 2005

Hoffmann 1939

Rudman 1972c

Hoffmann 1939 Perrier & Fischer 1911, Hoffmann 1939, Wägele & Klussmann-Kolb 2005 *Rudman 1972a

Previous histology (references)

12

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HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA

203

Phanerophthalmus smaragdinus (Rüppell & Leuckart 1828)

Smaragdinellidae +

+

Bulla vernicosa Gould, 1859

Bullidae

+

+

Haminoea cymbalum (Quoy & Gaimard, 1833)

+

0

+

+

+

?

0

0

0

0

0

0

0

+ *

0

0

0

0

0

0

0

0

+

0

0

+

0

+

0

+

0

+

+

Haminoea callidegenita Gibson & Chia, 1989

+

0

+

0

Haminoea antillarum (d’Orbigny, 1841)

+

Haminoea orteai Talavera, Murillo & Templado, 1987

Haminoeidae

Philinopsis cyanea (Martens, 1879)

Green algae (Rudman 1972d) (Rudman Web site Seaslugforum)

Diatoms, detritus, pieces of Ulva, Cladophora (Gibson & Chia 1989, own studies) Green algae (Rudman Web site Seaslugforum) Probably same food as other haminoids, namely turfing green algae (Burn & Thompson 1998) Green algae (Rudman Web site Seaslugforum)

Cephalaspidea (Rudman Web site Seaslugforum, Yonow 1992) Green algae (Rudman Web site Seaslugforum)

Unknown

Unknown **

MO (Spinella et al. 1992b, 1992c, 1993, Marín et al. 1999) **

SQ (Poiner et al. 1989, Fontana et al. 2001) **

OC (Spinella et al. 1998, Alvarez et al. 1998, Izzo et al. 2000) **

Unknown **

Unknown **

*Marcus 1957 (Bulla striata: discoidal glands above gill, open into mantle cavity)

Wägele & Klussmann-Kolb 2005, *Hoffmann 1939, *Marcus 1958, *Edlinger 1982

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DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS

Higher taxon

204

Cylichnidae

Philinidae

Diaphanidae

Genus and species, authorities

0

0

+

+

Acteocina atrata Mikkelsen & Mikkelsen, 1984 Sagaminopteron ornatum Tokioka & Baba, 1964

+

+

+

+

x

+

?

+

0

?

?

+

0

+

0

0

0

0

0

2 * 0

0

0

0

0

0

?

Foraminifera, Annelida, Crustacea, Mollusca, Echinodermata, (Rudman Web site Seaslugforum) Foraminifera

?Foraminifera (Cedhagen 1996)

?

0

Food (references)

10

Herbivore (Rudman 1972d)

Interpallial gland

Special defensive glands

9

0

3 Hypobranchial gland

+

4 Spongy mantel glands 0

5

Blochmann

+

6

Glandular stripe

+

8

7

MDF TYPE

Scaphander lignarius Lineus, 1758

Smaragdinella cf calyculata (Broderip & Sowerby 1829) Newnesia antarctica Smith, 1902 Philine alata Thiele, 1912

2

Column 1 MDF-like structures

Table 2 (continued) Compilation of available data on glandular structures, food and natural products

Unknown

Unknown

OC, IA? (Guiart 1901, Cimino et al. 1987a, 1989b) ***

Unknown ***

Unknown

PP OC (Szabo et al. 1996)

Natural products (references)

11

Odhner 1926, Jensen 1996 *Guiart 1901, *Thompson 1960, 1986, 1988, *Rudman 1972b (P. auriformis) “fossette glandulare” Perrier & Fischer 1911, Hoffmann 1939

Previous histology (references)

12

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HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA

Oxynoidae

SACOGLOSSA Plakobranchidae

Runcinidae

205 0

Thuridilla hopei (Verany, 1853)

+

0

Plakobranchus ocellatus van Hasselt, 1824

Oxynoe viridis (Pease, 1861)

0

0

Elysia ornata (Swainson, 1840)

Elysia viridis (Montagu, 1804)

0

+

+

Elysia crispata (Mörch, 1863)

Siphopteron quadrispinosum Gosliner, 1989 Runcina adriatica Thompson, 1980

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

+

+

0

0

+

0

0

3

0

0

0

0

0

0

0

0

0

+ *

0

0

0

Unusual contents of subepidermal glands

Many subepithelial glands

Derbesia tenuissima Green algae (Gavagnin et al. 1994c) Caulerpa (Jensen 1993)

Bryopsis sp. (Horgen et al. 2000, Jensen 1993) Codium vermilara, Bryopsis, Chaetomorpha Green algae (Jensen 1993, Gavagnin et al 1994, Trowbridge, 2004) Udotea, Chlorodesmis (Jensen 1993)

Caulerpa, Halimeda (Jensen 1993)

?

Unknown **

DT (Gavagnin et al. 1992, 1993, 1994c)

PP (Ireland & Scheuer 1979, Fu et al. 2000, Manzo et al. 2005)

PP (Gavagnin et al. 1992, 1994c) **

PP (Ireland et al., 1979, Ireland & Faulkner 1981, Ksebati 1985, Ksebati & Schmitz,1985, Gavagnin et al 1996, 1997a, 2000 (some as Tridachia crispata)) ** NC (Horgen et al. 2000) **

Unknown

Unknown

Kawaguti et al. 1966, Wägele & Klussmann-Kolb 2005

Thompson 1960, Wägele 1997

Klussmann-Kolb & Klussmann 2003 *Vayssiere 1883, *Hoffmann 1939, *FernandezOvies 1983 Hoffmann 1939 Wägele & Klussmann-Kolb 2005, *Marcus 1957 E. cauze

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DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS

Genus and species, authorities

Higher taxon

206

Akera soluta (Gmelin, 1791)

Aplysia parvula Guilding in Mörch, 1863)

Akeridae

Aplysiidae

ANASPIDEA

2

Column 1

0 0

+ ?

0 0

0

3 Hypobranchial gland

0

4 Spongy mantel glands

+

5

Blochmann +

6

Glandular stripe

+

7

MDF TYPE

+

8 MDF-like structures Opaline gland

Special defensive glands

9

Green and red algae, Delisea pulchra, Laurencia filiformis, Portieria hornemannii

Green algae (Rudman Web site Seaslugforum)

Food (references)

10

Table 2 (continued) Compilation of available data on glandular structures, food and natural products

MT DT SQ (Willan 1979, Fenical et al. 1979, Miyamoto et al. 1995, de Nys et al. 1996, Yamada & Kigoshi 1997, Higuchi et al. 1998, Rogers et al. 2000a,b, Ginsburg & Paul 2001, Jongaramruong et al. 2002)

Unknown **

Natural products (references)

11

Blochmann 1883, Perrier & Fischer 1911, Klussmann-Kolb 2004 *Perrier & Fischer 1911, *Hoffmann 1939, *Morton 1972 *Marcus & Marcus 1955, Klussmann-Kolb 2004

Previous histology (references)

12

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HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA

THECOSOMATA

207

Limacina helicina (Phipps, 1774) +

0

0

Bursatella leachii Blainville, 1817

Dolabrifera dolabrifera (Cuvier, 1817)

0

Aplysia punctata Cuvier, 1803

+

?

+

+

0

+

0

+

?

0

0

+

0

0

0

0

0

0

0

0

Opaline gland

Opaline gland

Opaline gland

Cyanobacteria (Rudman Web site Seaslugforum)

Plocamium coccineum, Enteromorpha, Laurencia sp. (Carefoot 1967, Quiñoá et al. 1989, Faulkner 1992)

TS (Baalsrud 1950)

OC NC (Fenical et al. 1979, Gopichand & Schmitz 1980, Schmitz et al. 1981, Cimino et al. 1987b, Racioppi et al. 1990, Kawamine et al. 1991, Scheuer 1992, Appleton et al. 2002) PP (Ciavatta et al. 1996a)

MT DT SQ TS NC OC (Minale & Riccio 1976, Castedo et al. 1983, Jiménez et al. 1986, Quiñoá et al. 1989, Ortega et al. 1997, Butzke et al. 2002, Findlay & Li 2002)

Blochmann 1883, Hoffmann 1939, Wägele & Klussmann-Kolb 2005 Hoffmann 1939

Blochmann 1883, Mazzarelli 1893, Hoffmann 1939, Merton 1920, Eales 1921, Wägele 1997, Wägele & Willan 2000, Klussmann-Kolb 2004

7044_book.fm Page 207 Friday, April 14, 2006 1:28 PM

DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS

Higher taxon

208

Umbraculidae

TYLODINOIDEA Tylodinidae 0

0

Umbraculum umbraculum (Lightfoot, 1786)

0

0

0

0 0

0

0

0

0

0

0

0

3 Hypobranchial gland

0

4 Spongy mantel glands 0

5

Blochmann

0

6

Glandular stripe

0

8

7

MDF TYPE

Tylodina perversa (Gmelin, 1791)

Clione limacina (Phipps, 1774)

Genus and species, authorities

GYMNOSOMATA

2

Column 1 MDF-like structures Dorsal mantle gland

Dorsal mantle gland

Opaline glandular cells

Special defensive glands

9

Geodia cydonium, Porifera (Cimino et al. 1988a, 1989a)

Aplysina aerophoba, Porifera (Cimino et al. 1990b, Becerro et al. 2003)

Thecosomata

Food (references)

10

Table 2 (continued) Compilation of available data on glandular structures, food and natural products

DG (Cimino et al. 1988a, 1989a, Gavagnin et al. 1990, De Medeiros et al. 1990, 1991 (some as U. mediterraneum)) ***

NC (Cimino et al 1986a, 1990b, Teeyapant et al. 1993, Ebel et al. 1999, Thoms et al. 2003)

TS TT (Baalsrud 1950, Fisher et al. 1956, McClintock & Janssen 1990, Yoshida et al. 1995, Bryan et al. 1995, McClintock & Baker 1997 (some as C. antarctica), Kattner et al. 1998)

Natural products (references)

11

Hoffmann 1939 Wägele & Klussmann-Kolb 2005, *Mazzarelli 1897, *MacFarland 1966 Vayssiere 1885, Wägele & Klussmann-Kolb 2005

Meisenheimer 1905, Hoffmann 1939 Hoffmann 1939, Wägele & Klussmann-Kolb 2005

Previous histology (references)

12

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HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA

NUDIBRANCHIA ANTHOBRANCHIA Bathydorididae

PLEUROBRANCHOIDEA Pleurobranchidae

209

0

0

Berthellina citrina (Rüppell & Leuckart 1828)

Berthellina edwardsii (Vayssière, 1896)

0

0

Bathydoris clavigera Thiele, 1912

Bathydoris hogdsoni Eliot, 1907

0

0

Berthella stellata (Risso, 1826)

Tomthompsonia antarctica (Thiele, 1912)

0

Bathyberthella antarctica Willan & Bertsch, 1987

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

Median buccal gland Subepithelial acid gland

Median buccal gland Subepithelial acid gland

Median buccal gland

Median buccal gland

Ceratoisis, Bryozoa, Crinoidea, Crustacea, Ophiuroidea (omnivore Wägele 1989a,c) Porifera, Ceratoisis, Bryozoa, Crinoidea, Crustacea, Ophiuroidea (omnivore Wägele 1989a,c, Avila et al. 2000)

Nonselective deposit feeder (Hain et al. 1993)

Porifera ?Anthozoa (Rudman Web site Seaslugforum)

Porifera (Rudman Web site Seaslugforum)

SQ (Iken et al. 1998, Avila et al. 2000)

Unknown

Unknown

IA ( Franc 1968, Thompson, 1969, 1970, Edmunds & Thompson 1972, Marbach & Tsurnamal 1973, Thompson & Colman 1984) IA OC (Avila 1992, 1993 (as B. aurantiaca))

IA (Avila 1992, 1993, Thompson & Colman 1984)

IA (Avila, unpublished data)

Hoffmann 1939 Wägele 1997

Wägele 1997

Wägele 1997, Wägele & Willan 2000 *Thompson 1960, *1969, Thompson & Colman 1984 Marbach & Tsurnamal 1973, Thompson & Colman 1984, Wägele & Klussmann-Kolb 2005

Hoffmann 1939

7044_book.fm Page 209 Friday, April 14, 2006 1:28 PM

DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS

Higher taxon

210

Goniodorididae

Ancula gibbosa (Risso, 1818) Goniodoris nodosa (Montagu, 1808) Trapania maculata Haefelfinger, 1960

Acanthodoris pilosa Abildgaard in Müller 1789 Onchidoris bilamellata (Linné, 1767)

Genus and species, authorities

Doridoidea Onchidorididae

2

Column 1

0

0 0 0

0

0 0 0

0

0 0 0

0

0

0

0

0

0

0

0

0

0

0

0

0

3 Hypobranchial gland

0

4 Spongy mantel glands

0

5

Blochmann 0

6

Glandular stripe

0

7

MDF TYPE

0

8 MDF-like structures Special defensive glands

9

Ascidiacea (McDonald & Nybakken Web site) Ascidiacea (McDonald & Nybakken Web site) Eudendrium, Ircinia, Porifera, Scrupocellaria, Bryozoa (McDonald & Nybakken Web site)

Balanidae, Bryozoa (McDonald & Nybakken Web site)

Bryozoa (McDonald & Nybakken Web site)

Food (references)

10

Table 2 (continued) Compilation of available data on glandular structures, food and natural products

Unknown **

Unknown

TS IA? (Herdmann & Clubb 1892, Edmunds 1968, Voogt 1970, 1972, 1973, Potts 1970, 1981, Thompson 1960) Unknown

Unknown **

Natural products (references)

11

Wägele & Cervera 2001 Wägele 1997

*Marcus 1959, Thompson 1960, Wägele 1997 Potts 1981, Thompson 1988, Wägele 1997, * Thompson 1960, *Edmunds 1968

Previous histology (references)

12

7044_book.fm Page 210 Friday, April 14, 2006 1:28 PM

HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA

Polycera quadrilineata (Müller, 1776) Polycerella emertoni Verrill, 1880 Roboastra gracilis (Bergh, 1877)

Polyceridae

Triophidae

Gymnodoris striata (Eliot, 1908)

Gymnodorididae

211

Crimora papillata Alder & Hancock, 1862 Laila cockerelli MacFarland, 1905 Limacia clavigera (Müller, 1776)

Thecacera pennigera (Montagu, 1815)

Corambe lucea Bergh, 1869

Corambidae 0

0

0 0 0

0

0

0 0 0

0 0 0

0 0

0 0 0

0 0 0 0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

+ * 2

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

Extremely glandular notum epithelium Many subepithelial glands, additional glands in cerata at gills

Bryozoa (McDonald & Nybakken Web site) Bryozoa (McDonald & Nybakken Web site) Bryozoa (Thompson & Brown 1984)

Bryozoa (McDonald & Nybakken Web site)

Plakobranchus, other opisthobranchs (McDonald & Nybakken Web site) Bryozoa (McDonald & Nybakken Web site) Bryozoa (McDonald & Nybakken Web site) Probably other polycerids (Pola et al. 2005)

Bryozoa (McDonald & Nybakken Web site)

NC (Graziani & Andersen 1998)

Unknown

Unknown

Unknown

Unknown **

Unknown

Unknown **

Unknown

Unknown

Wägele 1997, Wägele & Willan 2000

Wägele & Klussmann-Kolb 2005

Wägele 1997

Thompson, 1960, Wägele 1997

Marcus 1959, Schrödl & Wägele 2001, *Fischer 1892, *MacFarland & O’Donoghue 1929

7044_book.fm Page 211 Friday, April 14, 2006 1:28 PM

DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS

Genus and species, authorities

Higher taxon

212

Actinocyclus japonicus (Eliot, 1913) Archidoris pseudoargus (Rapp, 1827)

Dorididae

Austrodoris kerguelenensis (Bergh, 1884)

Aegires albus Thiele, 1912 Notodoris citrina Bergh 1875

Aegiridae

Plocamopherus ceylonicus (Kelaart, 1858)

2

Column 1

0

0

4 Spongy mantel glands 0

0

3 Hypobranchial gland

0

0

0

0

0

?

?

?

0

0

0

0

0

0

0

?

0

0

0

0

?

0

0

0

0

?

0

0

+

5

Blochmann

0

6

Glandular stripe 0

7

MDF TYPE

0

8 MDF-like structures 0

Median buccal gland 2 types of MDF-like structures 0

Special defensive glands

9

Rossella spp., Cynachira barbata, Porifera (Wägele 1989a, Iken et al. 2002)

Porifera (McDonald & Nybakken Web site)

Porifera/Calcarea (Wägele 1989a) Leucetta chagosensis, Porifera (McDonald & Nybakken Web site, Carmely et al. 1989)

Bryozoa (McDonald & Nybakken Web site)

Food (references)

10

Table 2 (continued) Compilation of available data on glandular structures, food and natural products

TS (Toyama &Tanaka 1956) TS TT DG (Cimino et al. 1993b, Zubía et al. 1993, Soriente et al. 1993, Armstrong et al. 2000 (see also Avila 1995)) DG (Davies-Coleman & Faulkner 1991, Avila 1995, Gavagnin et al. 1995, 1999a, 1999b, 2003a, 2003b, Iken et al. 2002)

NC (Carmely et al. 1989)

Unknown

Unknown

Natural products (references)

11

Potts 1981

Wägele 1997, *Kress 1981

Previous histology (references)

12

7044_book.fm Page 212 Friday, April 14, 2006 1:28 PM

HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA

0

Peltodoris atromaculata (Bergh, 1880)

0

0

Jorunna tomentosa (Cuvier, 1804)

Platydoris argo (Linneus, 1767)

0

Doris verrucosa Linné, 1758

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

Petrosia ficiformis, Haliclona (Reniera) fulva, Porifera (McDonald & Nybakken Web site, Castiello et al. 1978, 1980, Cimino et al. 1980b, 1982, Cattaneo-Vietti et al. 1993, 2001 Avila 1993, 1995, 1996, Gemballa & Schermutzki 2004) Porifera, Bryozoa (McDonald & Nybakken Web site, Megina et al. 2002)

Porifera (McDonald & Nybakken Web site)

Hymeniacidon sanguinea, Porifera (McDonald & Nybakken Website, Avila et al. 1990a, Avila 1993)

213

TS (Avila 1992, 1993)

AC TS (Voogt 1973, Castiello et al. 1978, 1980 Cimino et al. 1980b, 1981, 1982, 1985a, 1989c, 1990c Avila 1992, 1993)

DG TS NC (Cimino et al. 1986b, 1988c, Porcelli et al. 1989, Gavagnin et al. 1990, 1997b, Avila et al. 1990a, Pani et al. 1991, Avila 1992, 1993, De Petrocellis et al. 1991, 1996, Granato et al. 2000, Fontana et al. 2003 (but see also Avila 1995)) Unknown **

Wägele 1997, *Foale & Willan 1987 Avila 1993, Avila & Durfort 1996, Wägele 1997

Edmunds 1968, Avila 1993, Avila & Durfort 1996

7044_book.fm Page 213 Friday, April 14, 2006 1:28 PM

DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS

Higher taxon

Chromodorididae

Genus and species, authorities

Cadlina marginata MacFarland, 1905

Rostanga pulchra MacFarland, 1905

2

Column 1

0

0

0

3 Hypobranchial gland 0

0

4 Spongy mantel glands

0 1 0

0

5

Blochmann

0

6

Glandular stripe 0

7

MDF TYPE

0

8 MDF-like structures Glands in tubercles

Special defensive glands

9

Ophlitaspongia pennata, Porifera (McDonald & Nybakken Web site, Ong & Penney, 2001) Dysidea fragilis, D. amblia, D. etheria, D. herbacea, Dysidea sp., Axinella sp., Aplysilla glacialis, Porifera (McDonald & Nybakken Web site, Thompson et al. 1982, Hellou et al. 1982, Tischler & Andersen 1989)

Food (references)

10

Table 2 (continued) Compilation of available data on glandular structures, food and natural products

SQ DT ST (Hellou et al. 1981, 1982, Thompson et al. 1982, Walker 1982, Gustafson et al. 1985, Gustafson & Andersen 1985, Tischler & Andersen 1989, Tischler 1990, Faulkner et al. 1990, Tischler et al. 1991, Burgoyne et al. 1993, Dumdei 1994, Fontana et al. 1995, Dumdei et al. 1997a, Kubanek et al. 1997, 2000, Kubanek 1998 (but see also Avila 1995))

TT (Coulom 1966, Anderson 1971, 1973)

Natural products (references)

11

*Marcus 1955 (Cadlina rumia)

*Foale & Willan 1987

Previous histology (references)

12

7044_book.fm Page 214 Friday, April 14, 2006 1:28 PM

HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA

214

? ? 0

0 0

? ? 0

0 0

? ? 0

Chromodoris purpurea (Laurillard, 1831) Chromodoris tumulifera Collingwood, 1881 Chromodoris westraliensis (O’Donoghue, 1925) Glossodoris atromarginata (Cuvier, 1804) Glossodoris pallida (Rüppel & Leuckart, 1828) Glossodoris rufomarginata (Bergh, 1890)

Chromodoris krohni (Verany, 1846) Chromodoris luteorosea (Rapp, 1827) 0 0

215 0 0

0

0 0

0

?

0

0 0

0

?

0 0

?

0

0

0

Ceratosoma gracillimum (Semper in Bergh, 1876) Ceratosoma trilobatum (Gray J.E., 1827) Chromodoris britoi Ortea and Pérez, 1983

0

0

0

Cadlina laevis (Linneus, 1767)

0

?

0

0

0

0

0

0

0

?

?

0

3

+

3

3

1

3

3

3

3

+

+

1

0

?

0

0

0

0

0

0

0

?

?

0

ST (Rogers & Paul 1991, Avila & Paul 1997)

Cacospongia sp., Porifera (Avila & Paul 1997) Porifera (McDonald & Nybakken Web site)

ST (Gavagnin et al. 2004)

DT (Fontana et al. 1997, 1999b)

Unknown **

DT (Avila et al. 1990b, Avila 1992, 1993, 1995) DT (Avila et al. 1990b, Cimino et al. 1990a, Gavagnin et al. 1992, Puliti et al. 1992, Avila 1992, 1993, 1995) DT (Avila et al. 1990b, Avila 1992, 1993, 1995) Unknown **

DT (Avila 1993, 1995)

ST (Mollo et al. 2005)

ST (Mollo et al. 2005)

SQ, ST (Fontana et al. 1995)

Porifera (McDonald & Nybakken Web site)

Porifera (McDonald & Nybakken Web site)

Porifera (McDonald & Nybakken Web site) Porifera (McDonald & Nybakken Web site)

Porifera (McDonald & Nybakken Web site, Barbour 1979) Dysidea (Mollo et al. 2005) Dysidea (Mollo et al. 2005) Porifera (Avila 1993)

Avila & Paul 1997

García-Gómez et al. 1991

Avila 1993, Avila & Durfort 1996, *Marcus 1955 (Glossodoris) neona)

Wägele & Willan 2000

7044_book.fm Page 215 Friday, April 14, 2006 1:28 PM

DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS

Genus and species, authorities

Higher taxon

216 ? 0

? 0

? 0

0

0

Hypselodoris gasconi Ortea, 1996 Hypselodoris orsinii (Verany, 1846)

0

0

?

0

0

?

?

0

?

0

0

?

2

+

0

3

0

?

0

0

?

?

?

3 Hypobranchial gland

+

?

4 Spongy mantel glands

?

5

Blochmann

+

6

Glandular stripe ?

8

7

MDF TYPE

Hypselodoris fontandraui (Pruvot-Fol, 1951)

Hypselodoris bayeri (Marcus & Marcus, 1967) Hypselodoris bilineata (Pruvot-Fol, 1953) Hypselodoris cantabrica Bouchet & Ortea, 1980

2

Column 1 MDF-like structures Special defensive glands

9

Porifera (McDonald & Nybakken Web site) Dysidea fragilis, Porifera (McDonald & Nybakken Web site, Bouchet & Ortea 1980, Fontana et al. 1993) Dysidea avara, Porifera (Avila 1993, McDonald & Nybakken Web site) Dysidea, Porifera (Avila, 1993) Cacospongia mollior, Porifera (McDonald & Nybakken Web site, Cimino et al. 1973, 1974, 1982, 1993a, Avila 1993)

Food (references)

10

Table 2 (continued) Compilation of available data on glandular structures, food and natural products

SQ (Avila 1993 (as Hypselodoris sp)) ST (Cimino et al 1982, 1993a, Avila 1992, 1993)

SQ (Avila 1993)

SQ (Avila 1992, 1993, Fontana et al. 1993)

Unknown

SQ (Fontana et al. 1994b)

Natural products (references)

11

Avila 1993, Avila & Durfort 1996

García-Gómez et al. 1990, Avila 1993, Avila & Durfort 1996 García-Gómez et al. 1990, Wägele 1997

Previous histology (references)

12

7044_book.fm Page 216 Friday, April 14, 2006 1:28 PM

HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA

217 ?

0

0

0

Risbecia tryoni (Garrett, 1873)

0

0

?

0

Hypselodoris villafranca (Risso, 1818)

0

0

?

0

Hypselodoris tricolor (Cantraine, 1835)

0

0

Noumea cf. crocea Rudman, 1986

0

Hypselodoris picta (Schultz, 1836)

0

?

0

0

0

3

0

2

3

3

0

?

0

0

0

Porifera (McDonald & Nybakken Web site)

Dysidea fragilis, Fasciospongia cavernosa, (= Microciona toxystila), Pleraplysilla spinifera, Porifera (Avila 1993, Cimino & Sodano 1989, Avila et al. 1990b, 1991b, Fontana et al. 1994a,b) Dysidea fragilis, Porifera (McDonald & Nybakken Web site, Avila 1993, Fontana et al. 1993) Dysidea fragilis, Porifera (McDonald & Nybakken Web site, Cimino & Sodano 1989, Avila 1993, Avila et al. 1990b, 1991b)

Unknown

Unknown

SQ (Cimino et al. 1980b, 1982, Avila 1992, 1993, Cimino & Sodano 1989, Avila et al. 1990b, 1991b, Fontana et al. 1993)

SQ (Cimino et al. 1982, Avila 1992, 1993, Fontana et al. 1993, 1994b)

SQ (Cimino et al. 1982, Cimino & Sodano 1989, Avila 1992, 1993, Avila et al. 1990b, 1991b, Fontana et al. 1994a, b (some as H. webbi))

*Risbec 1953 (Noumea decussata) Wägele & Klussmann-Kolb 2005

García-Gómez et al. 1991, Wägele 1997, Wägele & Willan 2000 Avila 1993, Avila & Durfort 1996

García-Gómez et al. 1990 (as H. webbi), García-Gómez et al. 1991 (as H. elegans), Avila 1993, Avila & Durfort 1996 (as H. webbi)

7044_book.fm Page 217 Friday, April 14, 2006 1:28 PM

DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS

Higher taxon

218 0

0

0

Dendrodoris nigra (Stimpson, 1855)

Doriopsilla gemela Gosliner, Schaefer & Millen, 1999 0

0

0

0

0

0

0

3 Hypobranchial gland

0

0

0

0

0

0

+

0

0

0

0

4 Spongy mantel glands

0

5

Blochmann 0

6

Glandular stripe

0

8

7

MDF TYPE

Dendrodoris limbata (Cuvier, 1804)

Dendrodoris grandiflora (Rapp, 1827)

Genus and species, authorities

Dendrodorididae

2

Column 1 MDF-like structures Special defensive glands

9

Porifera (McDonald & Nybakken Web site)

Ircinia fasciculata, Fasciospongia cavernosa (= Microciona toxystila), Spongia officinalis, Porifera (McDonald & Nybakken Web site, Cimino et al. 1975, 1980b, 1982, 1985a, 1986a, 1990b) Porifera (McDonald & Nybakken Web site)

Food (references)

10

Table 2 (continued) Compilation of available data on glandular structures, food and natural products

Unknown **

SQ (Cimino et al 1981, 1982, 1983, 1985b, 1986a, 1988b, Avila 1992, 1993, Avila et al. 1991a, Fontana et al. 1999a, 2000) SQ (Okuda et al. 1983)

SQ ST MO OC (Cimino et al. 1980b, 1982, 1985a, 1986a, 1988b, 1990b, Avila 1992, 1993, Avila et al. 1991a, Fontana et al. 1999a, 2000)

Natural products (references)

11

Wägele 1997, Wägele et al. 1999

Avila 1993, Avila & Durfort 1996

*Brodie 2005

Previous histology (references)

12

7044_book.fm Page 218 Friday, April 14, 2006 1:28 PM

HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA

CLADOBRANCHIA Dendronotoidea Tritoniidae

DEXIARCHIA Doridoxidae (1)

Phyllidiidae

219 0

0

Tritonia festiva (Stearns, 1873)

Tritonia plebeia Johnston, 1828 0 0

0

0

0

?

0

0

0

0

0

0

Tritonia antarctica Pfeffer in Martens & Pfeffer, 1886 Tritonia challengeriana Bergh, 1884

0

0

Marionia blainvillea (Risso, 1818) 0

0

?

?

0

0

0

?

?

0

0

0

0

0

?

Phyllidiella pustulosa (Cuvier, 1804)

Doridoxa ingolfiana Bergh, 1899

0

Phyllidia flava Aradas, 1847

0

0

0

0

0

0

?

0

0

0

0

0

0

0

?

0

Violet glands in epidermis

Violet glands grouped and sunken into notum Violet glands in epidermis

Violet glands in epidermis

Octocorallia (McDonald & Nybakken Web site) Octocorallia (McDonald & Nybakken Web site)

Octocorallia (McDonald & Nybakken Web site)

Axinella, Porifera (Cimino et al. 1982, unpublished data of HW) Acanthella cavernosa, Densa sp., Halichondria cf lendenfeldi, Phakellia carduus (Karuso 1987, Fusetani et al. 1991, Kassühlke et al. 1991, Dumdei et al. 1997b, Wright 2003)

NC (Kennedy & Vevers 1953)

Unknown

Unknown

Unknown

Unknown

Unknown

SQ (Cimino et al. 1982, 1986a (as P. pulitzeri) (but see also Avila 1995)) ** SQ, DT (Karuso 1987, Kassühlke et al. 1991, Fusetani et al. 1991, 1992, Okino et al. 1996, Hirota et al. 1998, Dumdei et al. 1997b, Simpson et al. 1997, Garson et al. 2000, Wright 2003, Manzo et al. 2004)

Wägele & Klussmann-Kolb 2005 *Thompson 1960, *Marcus 1959 (as T. australis)

Hoffmann 1939

Wägele 1997

7044_book.fm Page 219 Friday, April 14, 2006 1:28 PM

DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS

220

Bornellidae

Dotidae

Lomanotidae

Dendronotidae

0 0

0 0

0

0

0

0

+

+

0 0

+

0

0

0

0

0

0

0

0

0

0

Dendronotus iris Cooper, 1863

Lomanotus vermiformis Eliot, 1908 Doto coronata (Gmelin, 1791) Bornella anguilla Johnson, 1984 Bornella stellifer (Adams & Reeve in Adams, 1848)

0

Dendronotus frondosus (Ascanius, 1774)

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

3 Hypobranchial gland

0

0

4 Spongy mantel glands

0

5

Blochmann

Tritoniella belli Eliot, 1907

Higher taxon

6

Glandular stripe

0

Genus and species, authorities

8

7

MDF TYPE

Tritonia vorax Odhner, 1926

2

Column 1 MDF-like structures Violet glands in epidermis Violet glands in epidermis Violet glands in epidermis Violet glands in epidermis

Violet glands in epidermis

Special defensive glands

9

Octocorallia (McDonald & Nybakken Web site) Octocorallia, Synascidia (McDonald & Nybakken Web site) Hydrozoa, Octocorallia, Hexacorallia, Bryozoa (McDonald & Nybakken Web site) Hexacorallia (McDonald & Nybakken Web site) Hydrozoa (McDonald & Nybakken Web site) Hydrozoa (McDonald & Nybakken Web site) Hydrozoa (McDonald & Nybakken Web site) Hydrozoa (McDonald & Nybakken Web site)

Food (references)

10

Table 2 (continued) Compilation of available data on glandular structures, food and natural products

Unknown

Unknown

Unknown

Unknown

Unknown

TS (Buznikov & Manukhin,1962, Voogt 1970, 1972, 1973)

OC (McClintock et al. 1994, Bryan et al. 1998)

Unknown

Natural products (references)

11

Vayssière 1888, Wägele 1997

Wägele 1997

Wägele 1997

Previous histology (references)

12

7044_book.fm Page 220 Friday, April 14, 2006 1:28 PM

HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA

Melibe leonina (Gould, 1853)

Crosslandia viridis Eliot, 1903

Tethydidae

Scyllaeidae

221

Charcotiidae

0

0

0

0

0 0

0

0

Dermatobranchus semistriatus Baba, 1949 Charcotia granulosa Vayssière, 1906 0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

Dermatobranchus sp.

Armina neapolitana (Delle Chiaje, 1824) Armina tigrina Rafinesque, 1814

Armina maculata Rafinesque, 1814

Phylliroe bucephala Peron & Lesueur, 1810

Phylliroidae

Arminoidea Arminidae

Hancockia uncinata (Hesse, 1872)

Hancockiidae

+

0

0

0

0

0

0

0

0

+

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

+

+

0

0

Marginal sacs

Marginal sacs

Marginal sacs

Marginal sacs

Marginal sacs

Two different MDF-like structures

Bryozoa (Barnes & Bullough 1996)

Octocorallia (McDonald & Nybakken Web site) Unknown

Veretillum cynomorium, Octocorallia (McDonald & Nybakken Web site, Guerriero et al. 1987, 1988, 1990)

Hydrozoa (Rudman Web site Seaslugforum)

Medusae of Hydrozoa, Appendicularia (McDonald & Nybakken Web site) Crustacea larvae (McDonald & Nybakken Web site)

Hydrozoa (McDonald & Nybakken Web site)

Unknown

Unknown

Unknown

Unknown

Unknown

DT (Guerriero et al. 1987, 1988, 1990)

MT TS (Ayer & Andersen 1983, Gustafson & Andersen 1985, Barsby et al. 2002) Unknown

Unknown

Unknown

Wägele et al. 1995a, Wägele & Willan 2000

*Wägele & Willan 2000

Wägele 1997

Kolb 1998

Kolb 1998, *Bergh 1866

*Thompson & Crampton 1984 (M. fimbriata)

*Thompson 1972 (H. burni), *Marcus 1957 (H. ryrca) Born 1910, Hoffmann 1939

7044_book.fm Page 221 Friday, April 14, 2006 1:28 PM

DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS

222

Aeolidoidea Notaeolidiidae

Madrellidae

Zephyrinidae

Dironidae

Notaeolidia depressa Eliot, 1907

Janolus mokohinau Miller & Willan, 1986 Madrella ferruginosa Alder & Hancock, 1864 0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

+

+

0

0

?

+

+

+

+

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

3 Hypobranchial gland

0

4 Spongy mantel glands 0

5

Blochmann

Pseudotritonia gracilidens Odhner, 1944 Pseudotritonia quadrangularis Thiele, 1912 Dirona albolineata MacFarland, 1912 Janolus capensis Bergh, 1907 Janolus cristatus (Delle Chiaje, 1841)

Higher taxon

6

Glandular stripe

0

Genus and species, authorities

8

7

MDF TYPE

Pseudotritonia antarctica (Odhner, 1934)

2

Column 1 MDF-like structures Special defensive glands

9

Actiniaria (Wägele 1990)

Bryozoa (McDonald & Nybakken Web site) Bryozoa (McDonald & Nybakken Web site)

Bryozoa (McDonald & Nybakken Web site) Bryozoa (McDonald & Nybakken Web site)

Bryozoa

Bryozoa (Barnes & Bullough 1996) Unknown

Unknown

Food (references)

10

Table 2 (continued) Compilation of available data on glandular structures, food and natural products

Unknown

Unknown

NC (Sodano & Spinella 1986, Cimino et al. 1986a, Giordano et al. 2000) Unknown

Unknown

Unknown

Unknown

Unknown

Unknown

Natural products (references)

11

Wägele 1997

*Baba 1935 (M. sanguinea)

Trinchese 1881, Hoffmann 1939

Wägele 1991 (as Telarma antarctica) Wägele 1991, Wägele 1997

Previous histology (references)

12

7044_book.fm Page 222 Friday, April 14, 2006 1:28 PM

HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA

223

0

0

0 0

0 0

Cerberilla amboinensis Bergh, 1905 Protaeolidiella juliae Burn, 1966

0

0

Aeolidia papillosa (Linneus, 1761)

0

0

Aeolidiidae

0

0

0

0

0

0

0

0

0

0

Calma glaucoides (Alder & Hancock, 1854)

Calmella cavolinii (Verany, 1846)

Flabellina babai Schmekel, 1973 Flabellina falklandica Eliot, 1907 Flabellina gracilis (Alder & Hancock, 1844) Flabellina pedata (Montagu, 1815)

0

0

Notaeolidia schmekelae Wägele, 1990 Flabellina affinis (Gmelin, 1791)

0

Calmidae

Flabellinidae

0

Notaeolidia gigas Eliot, 1905

+

0

0

0

0

0

0

+

0

0

+

0

+

+

0

0

+

+

+

+

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

Hydrozoa (McDonald & Nybakken Web site)

Hydrozoa (McDonald & Nybakken Web site) Eudendrium and other hydrozoans (Thompson & Brown 1984) Hydrozoa, ?Octocorallia (McDonald & Nybakken Web site) Eggs of blenniid fish (Calado & Urgorri 2001) Hexacorallia (McDonald & Nybakken Web site) Probably unknown

Hydrozoa (McDonald & Nybakken Web site)

Octocorallia (McDonald & Nybakken Web site) Actiniaria (Wägele 1990) Eudendrium sp., Hydrozoa (McDonald & Nybakken Web site, Cimino et al. 1980a, b)

Unknown

Unknown

OC (Rogers, 1977, Howe & Harris 1978)

Unknown

Unknown

Unknown

Unknown

Unknown

Unknown

TS (Cimino et al. 1980a,b)

Unknown

Unknown

Wägele 1997

Hoffmann 1939, Streble 1968

Evans 1922

Wägele 1997, Schulze & Wägele 1998

Wägele 1997

Wägele 1997, *Trinchese 1881 (several Flabellina species), *Marcus du BoisReymond 1970

Wägele et al. 1995b

7044_book.fm Page 223 Friday, April 14, 2006 1:28 PM

DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS

Higher taxon

0 0

0

0

0

224 0

0

Phyllodesmium guamensis Avila et al., 1998

Phyllodesmium jakobsenae Burghardt & Wägele, 2004

?

+

0

?

0

0

0

0

0

0

0

0

0

0

0

0

0

0

3 Hypobranchial gland

+

4 Spongy mantel glands 0

5

Blochmann

0

6

Glandular stripe

0

8

7

MDF TYPE

0

Phidiana lottini (D´Orbigny, 1847) Phyllodesmium briareum (Bergh, 1896)

Cratena peregrina (Gmelin, 1791)

Genus and species, authorities

Facelinidae

2

Column 1 MDF-like structures Special defensive glands

9

Eudendrium sp., Hydrozoa (McDonald & Nybakken Web site, Cimino et al. 1980a, b) Hydrozoa (McDonald & Nybakken Web site) Briareum, Octocorallia (McDonald & Nybakken Web site, Burghardt et al. 2005) Sinularia maxima, S. polydactyla, Sinularia sp., Octocorallia (Avila et al. 1998, Slattery et al. 1998, McDonald & Nybakken Web site) Octocorallia (Xenia) (Burghardt & Wägele 2004)

Food (references)

10

Table 2 (continued) Compilation of available data on glandular structures, food and natural products

Unknown

DT (Avila et al. 1998, Slattery et al. 1998)

Unknown

Unknown

TS (Cimino et al. 1980a,b, Ciavatta et al. 1996b)

Natural products (references)

11

Wägele 1997, Avila et al. 1998

Wägele 1997 (as P. indica) Wägele 1997, *Rudman 1981b

Previous histology (references)

12

7044_book.fm Page 224 Friday, April 14, 2006 1:28 PM

HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA

225

Siphonariidae

PULMONATA Onchidiidae

Tergipedidae

0

Onchidium verruculatum (Cuvier, 1830) 0

0

Onchidella borealis Dall, 1871

Siphonaria javanica (Lamarck 1819)

0

0

0

0

0

0

0

Onchidella celtica (Cuvier, 1817)

Tergipes tergipes (Forskål, 1771)

Eubranchus exiguus (Alder & Hancock, 1848) Cuthona caerulea (Montagu, 1804)

Eubranchidae

Glaucidae

Piseinotecus gabinieri (Vicente, 1975) Glaucus atlanticus Forster, 1777

Piseinotecidae

Pteraeolidia ianthina (Angas, 1865)

0 0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0 0

0

0

0

0

0

0

+

0

+

?

0

0

0

0

0

0

0

0

0

0

0

0

+

0

+

+

0

0

0

0

0

0

Many repugnatorial glands

Cyanobacteria (www.hku.hk/ecology/ porcupine/por28/ 28-glance-siphonaria. htm#index2)

Live algae (Stanisic 1998)

Live algae Diatoms, detritus, bacteria (Stanisic 1998) www.seanature.co.uk/ marine-education/ onchidella.htm Live algae (Stanisic 1998)

Octocorallia Hydrozoa (McDonald & Nybakken Web site) Hydrozoa (McDonald & Nybakken Web site) Hydrozoa, Siphonophora (McDonald & Nybakken Web site) Hydrozoa (McDonald & Nybakken Web site) Hydrozoa (Thompson & Brown 1984, McDonald & Nybakken Web site) Hydrozoa (McDonald & Nybakken Web site)

PP (Ireland et al. 1984, Arimoto et al. 1990, 1993) Unknown **

OC ** (Young et al. 1986, Abramson et al. 1989)

Unknown **

Unknown

TT (Bürgin-Wyss 1961 (as Trinchesia))

Unknown

Unknown

Unknown

Unknown

Young et al. 1986, Weiss & Wägele 1998 *Marcus du BoisReymond 1971

Marcus du BoisReymond 1979 (several species), Weiss & Wägele 1998

Trinchese 1877, Wägele 1997

Hoffmann 1939, Edmunds 1966a *Edmunds 1966a, *Rudman 1981a

Rudman 1982, Wägele 1997

7044_book.fm Page 225 Friday, April 14, 2006 1:28 PM

DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS

Higher taxon

226

0 0

3 Hypobranchial gland

0

4 Spongy mantel glands 0

5

Blochmann

0

6

Glandular stripe

+

8

7

MDF TYPE

Special defensive glands

9

Pyramidellids are ectoparasites on various polychaetes, bivalves and other gastropods (Ponder & de Keyzer 1998)

Food (references)

10

Unknown

Natural products (references)

11

Wise 1996

Previous histology (references)

12

Notes: All species listed have been re-investigated by histological means, except for the members of the Chromodorididae, where only a few species have been investigated. For a compilation of all available data on presence or absence of MDFs in Chromodorididae see Table 3. A question mark indicates lack of data, due to inappropriate histological slides or because of lack of literature data. Column 7: * indicates that only one or two MFDs were found. Column 8: * indicates that only one to four MDF-like structures were observed. Column 9: indicates special glandular structures, which are typical of only a small group. Column 10: indicates the food preference. Very often, only the general groups of prey are known. Whenever possible, details of genera or species are given. Column 11: summarises known natural products. The category of the substance is given, instead of the names of the products, as follows: AC acetylenes, DG diacylglycerols, IA inorganic acids, MO compounds with mixed origin, MT monoterpenes, DT diterpenes, SQ sesquiterpenes, ST sesterterpenes, TS triterpenes and steroids, TT tetraterpenes, NC nitrogenated compounds, OC other compounds, PG prostaglandins and eicosanoids, PP polyproprionates. ** indicates that other species of the same genus have been chemically studied. *** Philine alata, Scaphander lignarius and Umbraculum umbraculum do not produce an acid secretion (Avila, unpublished data). Column 12: References including previous histological investigations and pictures on probably defensive glandular structures. *indicates that other species of the same genus are described.

Pyramidella sulcata Adams, 1854

Genus and species, authorities

HETEROBRANCHIA Pyramidellidae

2

Column 1 MDF-like structures

Table 2 (continued) Compilation of available data on glandular structures, food and natural products

7044_book.fm Page 226 Friday, April 14, 2006 1:28 PM

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DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS

Figure 1 Histological sections of opisthobranch epidermal and subepithelial glands. (A) Marionia blainvillea epidermis. (B) Dendrodoris nigra epidermis; Arrow: single glands with acid mucopolysaccharides, asterisk: homogenously light blue stained glandular cell. (C) Acteon tornatilis spongy glands, note the invagination of the epithelium. (D) Chelidonura ornata, hypobranchial gland (arrow) and spongy tissue (asterisk). (E) Thuridilla hopei subepithelial glands with crystalline structures. (F) Chelidonura pallida glandular stripe, note the duct of one of the cells (arrow). (G) Akera soluta glandular stripe, note the small duct (arrow). Scale bars in µm.

In a few species, cells are present which have a large vacuole with homogenously staining light blue contents (Figure 1B, Dendrodoris nigra, asterisk). Spongy glands at mantle rim. (Table 1, Table 2 Column 4) This gland is also called “Mantelranddrüsen” (Hoffmann 1939), or “glande semi-lunaire” (Pelseneer 1888, 1894). Several members of the Opisthobranchia, belonging to many different groups, show these spongelike vacuolated cells. The cells are very large, with a tiny nucleus. The single large vacuole does not stain (Figure 1C, Acteon tornatilis). The cells are actually epithelial cells but, due to their size, they can come to lie subepthelial in comparison with the other epithelial cells. Due to invagination of the epidermis, the glandular cells lie in saclike depressions. In many species, these glands are located near to the mantle edge and can be clearly identified by their kind of pores, which are formed by the invagination of the epidermis. This glandular epithelium is restricted to the mantle rim in members of 227

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the Acteonoidea, Cephalaspidea sensu stricto and Anaspidea. Some dorids, like Trapania and Polycera have an outer epithelium, which seems to be spongy, but the size of the glandular cells is smaller, and the contents are stained lightly bluish. In several opisthobranchs (Chelidonura, Ancula) the notum beneath the epithelium appears spongy due to large cells with a tiny nucleus and a huge nonstaining vacuole (Figure 1D, Chelidonura ornata, asterisk). In these cases, however, no openings through the epidermis could be observed. Therefore, this type of cell is not considered to be homologous with the spongy glandular epithelium shown in Figure 1C. Hypobranchial gland. (Table 1, Table 2 Column 3) This gland consists of elongate epidermal cells which stain light violet to red. They form a compact layer, with tiny supporting cells interspersed (Figure 1D, Chelidonura inornata, arrow). In some cephalaspidean species, this gland is voluminous and secretes copious amounts of mucus (e.g., in Haminoea callidegenita). Sometimes, this glandular layer is reduced to few cells interspersed with ordinary epithelial cells. When the locality and staining properties of these few cells are identical to the typical hypobranchial gland in other opisthobranchs, these glandular cells are considered to be a hypobranchial gland. This gland is mainly found in species which still have a mantle cavity (e.g., many Cephalaspidea). Subepithelial glands (Table 1) Subepithelial single glands producing acid mucopolysaccharides (staining violet to red). (Table 1) The single cells have a drop-like structure with their duct-like part running between the epidermal cells and opening to the outside. The cells stain violet. These glands are widespread in many Opisthobranchia and probably are one of the major glandular structures (Figure 4B, Thecacera pennigera). Some species (e.g. Elysia crispata) are completely covered by this type of gland. In Thuridilla hopei, the contents of the cells resemble small globular crystals (Figure 1E). This is rather unusual and was observed only in this species. Opaline gland (gland of Bohadsch, grape-shaped gland) (Table 1, Table 2 Column 9) The opaline gland lies beneath the ventral floor of the mantle cavity. The cells are considerably larger than the normal subepithelial cells and open to the outside with a small pore each. They also have a large nucleus (Figure 2D arrow, Bursatella leachii). In a few aplysiids only, the single glandular cells open into a common duct, which leads to the outside. The opaline gland is considered to be present only in Anaspidea. Similar glands have been detected in members of the Gymnosomata (Figure 2E arrow, Clione limacina). They are also considered to be opaline glands. Supepithelial single gland cells staining bluish (cellules spéciales, glandular stripe) (Table 1, Table 2 Column 6 as glandular stripe). The contents of these cells stain bluish, the nucleus is of moderate size (Figure 1F, G). Sometimes a duct leading to the outside can be observed (Figure 1F, G arrows). These supepithelial glandular cells are widespread in some taxa (e.g., Anaspidea, Cladobranchia) but are missing in others (e.g., Doridoidea). In gill-bearing opisthobranchs, like cephalaspids and anaspids, the position of the glandular cells is related to the gill. The glands are usually found in the hyponotum, the ventral side of the notum covering and protecting the gill. In gill-less species (mainly the Cladobranchia) the glandular cells are arranged into a longitudinal stripe starting behind the genital papilla on the right side and running to the end of the lateral mantle side. In some species (e.g., Dirona) the glands are also located in a stripe on the left side. In some cerata-bearing animals, the glandular cells can be found at the base of the cerata (Doto, Eubranchus). Blochmann’s glands and ink gland (purple gland) (Table 1, Table 2 Column 5) Blochmann’s gland is a large single glandular cell lying subepithelially and characterised by a big nucleus. The contents hardly stain. The single gland has a duct composed of small cuboidal cells leading to the outside. The glandular cell is surrounded by muscle fibres. This glandular type is only present in some members of the Cephalaspidea (e.g., Figure 2A, Haminoea antillarum, Figure 2B, Bulla vernicosa) and Anaspidea. In Anaspidea this gland is called the ink gland and is composed of many Blochmann’s 228

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DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS

Figure 2 Histological sections of opisthobranch subepithelial glands. (A) Haminoea antillarum Blochmann’s gland with duct composed of cuboidal small cells. (B) Bulla vernicosa Blochmann’s gland. (C) Aplysia parvula ink gland (composed of Blochmann’s glands). (D) Bursatella leachii opaline gland (gland of Bohadsch), note the large nucleus (arrow). (E) Clione limacina opaline glands (gland of Bohadsch), note the large nucleus (arrow). (F) Cadlina laevis compound glands lying in notum with outleading duct. (G) Berthellina edwardsii acid glands in notum with opening to the outside. Scale bars in µm.

glands lying close together in the dorsal mantle cavity and opening above the gill (Figure 2C, Aplysia parvula). The ink gland exudes whitish or purple secretions. The ink gland is considered to be only present in Anaspidea, but it is difficult to differentiate between the ink gland in the Anaspidea and the presence of the Blochmann’s glands in several members of the Cephalaspidea. Subepithelial acid glands (Table 1, Table 2 Column 6) Huge subepithelial acid glands are present in some members of the Pleurobranchoidea (Berthellina). These structures can have a diameter of ~500 µm. The glands are composed of very few cells and lead to the outside (Figure 2G). Their contents do not stain, or only small pale patches are present. 229

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Other subepithelial glands composed of several cells These compound glands have larger vacuoles with granular and bluish stained contents. They have been observed in several species, e.g., Cadlina luteomarginata and C. laevis (Figure 2F). In the latter species, the glands are sunk deeply in the notum, and could also be assigned to the notum glands (see below). Glandular organs lying in the notum (Table 1, Table 2 Column 9) Dorsal mantle gland This gland is present in members of the Tylodinoidea. Although the position is similar in the two investigated species, Tylodina perversa and Umbraculum umbraculum, the morphology and histology are different. In both species, the gland is located in the dorsal notum tissue and it opens to the outside above the mouth area. U. umbraculum (Figure 3A) has a highly branched system of many tubules. Glandular tissue is only present in the finer tubules (Figure 3A, arrows). These connect to bigger tubules, which are surrounded by flat to cuboidal cells with no glandular vacuoles (Figure 3A, asterisks). The whole gland opens above the mouth in the mantle rim via one or two openings. Tylodina perversa (Figure 3B, C) has huge glandular follicles which stain grainy and in a greyish colour (asterisks). They seem to fuse in the anterior part of the mantle rim and form a large reservoir of secretion. Part of the gland has bigger cells with uniform violet contents (arrows). These areas are more confined to the dorsal part of the mantle and form several distinct ducts which open separately to the outside. Interpalleal gland The interpalleal gland in the genus Scaphander is roundish in its general appearance (Figure 3D). It is composed of many tiny tubules. These run together into a common duct, which opens in the outer part of the dorsal mantle cavity (Figure 3D and E, arrows). The cells lining the tubules are small, with a large vacuole. Their rather transparent contents stain light bluish. Marginal sacs of Arminidae These glandular and saclike structures are very conspicuous and arranged in the mantle rim of the animals. The glands are large (up to 1 mm), globular and composed of many cells which more or less stretch from the margin to the middle of the globes. The single vacuole contains a homogenously dark violet-stained substance. Nuclei are not visible in mature marginal sacs. The sacs are surrounded by a thin layer of muscular tissue (Figure 4A, Dermatobranchus semistriatus). These glandular structures only occur in members of the Arminidae and their staining properties are listed in Table 4 (see page 245). Agglomeration of glandular cells in ceratal processes or tubercles. Thecacera pennigera (Figure 4B) and Cadlina luteomarginata (Figure 4C) have glandular tissues, which are characterised by nonstaining vacuolated cells. These glands, which can easily be overlooked, are probably not homologous. In Thecacera pennigera the glands are arranged like a flower and were only observed in the ceratal processes next to the gill. In Cadlina luteomarginata the glandular tissue is located in the apical parts of the tubercles. Mantle dermal formations (MDF types) (Table 1, Table 2 Column 7, Table 3 and Table 4) Basically, MDFs are globular structures of usually >300 µm and are composed of many cells, each with a single large vacuole. Very often, especially within the Chromodorididae, these vacuoles do not stain with toluidine blue. The whole organ can be surrounded by a thin or rather thick layer of muscles (Table 3). MDFs are widely distributed in members of the doridoidean family Chromodorididae, but are also observed in members of other opisthobranch taxa (Table 2 Column 7). Whereas some of these taxa have MDFs rather regularly arranged (Chromodorididae, Limacia clavigera, Plakobranchus ocellatus), some seem to have only a few irregularly arranged MDFs (Newnesia antarctica, Elysia ornata, Haminoea orteai). Their appearance can vary to a great extent even within the same genus. At least three different types can be distinguished. Type 1 (Figure 5A, B) is characterised by the presence of a duct which leads to the outside. It is present in Cadlina luteomarginata, which has a specialised duct (Figure 5B) and in Chromodoris 230

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DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS

Figure 3 Histological sections of opisthobranch glands lying in the notum. (A) Umbraculum umbraculum cross section of anterior part of body with dorsal mantle glands. To the left more fine tubules with dark violet staining glandular cells are visible (arrows), whereas to the right, ducts with a wide lumen are more common (asterisks). (B) Tylodina citrina cross section through frontal part with the dorsal mantle separated from the underlaying body wall. Dorsal mantle glands with glandular ducts leading separately to the outside (arrow); greyish part of gland, which is connected to the glandular ducts marked with an asterisk. (C) Detail of Tylodina citrina dorsal mantle glands. Connection between greyish staining part (asterisk) to the violet staining part (arrow). (D) Scaphander lignarius interpalleal gland with main collecting duct, which leads to the outside (arrow) at the ventral part of dorsal notum. (E) Scaphander lignarius detail of interpalleal glands. Arrows indicate small ducts leading into main duct. Scale bars in µm.

tumulifera (Figure 5A), where the MDF is located beneath the epidermis and the vacuoles reach the outside. Type 2 (Figure 5C–F, Figure 6A) is characterised by a muscular clot which connects the MDF to the outside (see Table 3, e.g., Hypselodoris orsinii, Limacia clavigera). The clot is composed of muscle fibres which are arranged parallel to the epidermis and the MDF (Figure 5C, D, F). 231

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Figure 4 Histological sections of opisthobranch glands lying in the notum. (A) Dermatobranchus semistriatus marginal sac. Note the orientation of the cell vacuoles to the centre of the globe. (B) Thecacera pennigera glandular agglomerations in ceratal processes next to gills (arrows). At bottom of picture, subepithelial glands staining dark violet visible. (C) Cadlina luteomarginata glandular agglomerations in the apical parts of tubercles. (D) Bathyberthella antarctica acid glands. Note the tubular structure. (E) Plocamopherus ceylonicus acid glands in visceral cavity. Note the tubular structure and similar size as in Bathyberthella antarctica. (F) Plocamopherus ceylonicus acid glands in visceral cavity. Scale bars in µm.

Newnesia antarctica also has MDFs in its mantle, although these are not regularly arranged along a rim, but are rather clumped together. Nevertheless, these MDFs also show a muscular clot, with fibres arranged parallel to the epidermis (Figure 6A). Type 3 (Figure 6G, Figure 7A–F) seems to be independent of the outer epithelium and most of the MDFs investigated here were of this type. The density of the vacuoles may differ greatly, as does the muscle layer surrounding the MDF in the species investigated. For example, the density 232

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DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS

of vacuoles is very low in Glossodoris atromarginata (Figure 7D) and Plakobranchus ocellatus (Figure 7F) and there is nearly no muscle layer around their MDFs. Between the vacuolated cells, connective tissue is present. In contrast, the vacuoles are packed very densely in Hypselodoris tricolor (Figure 6G) and Risbecia tryoni (Figure 7C) and the muscle layer surrounding the MDF is very thick (40 µm, see Table 3). The MDF of Chromodoris westraliensis (Figure 7A) is peculiar because it does not show a muscular layer but a homogenously stained layer of unknown contents. The MDFs in C. westraliensis were the only ones with a flattened appearance. Vacuolated cells are rather sparse and arranged along the periphery. These cells are connected with the surrounding layer (Figure 7A, asterisk). MDFs in Laila cockerelli (Figure 7B) are rare and located in the ceratalike structures of the notum rim. Only two were recognised in the specimen investigated. The distribution of the MDFs in the organism is also variable between species and the difference in distribution in adult specimens of several species is shown in Figure 8. The main areas covered in most species are the mantle border, or especially near gills and rhinophores. However, Limacia clavigera has MDFs in all processes except those next to the gills. Histochemical analysis showed some differences in the MDFs of five chromodorid species investigated (Table 4). Even applying different staining techniques, the contents of the vacuoles never stained, whereas the surrounding layers of Chromodoris westraliensis, Hypselodoris tricolor and Limacia clavigera stain similarly as connective tissue (green in trichrome after Goldner and blue in trichrome Azan after Heidenhain), but not as muscles (which in both methods stain red). Unfortunately no information is available for the muscular clot. Table 2 contains additional information on the presence of MDFs taken from the literature combined with data obtained by the authors, although information on the size and description of MDFs is lacking for most species. Also, for these species no information on the presence of ducts leading to the outside, or on muscular clots was available and so the presence of these structure is only noted with a +. Similarly, for those species possessing MDFs, data on the presence and thickness of a muscular layer, and the presence or absence of a muscular clot, for example, are lacking (Table 3), because notes on MDFs are frequently not accompanied by any description or morphometrical data. As far as it is known, all the available data on presence/absence or descriptive details of MDFs are included in Table 2 and Table 3. MDF-like structures (Table 1, Table 2, Column 8) (Figure 6B, D, Figure 9A–F) There are several other glands similar to the MDFs but they differ in the number of cells, size and/or staining properties. The structures observed in Doriopsilla gemela (Figure 6B) are quite similar to true MDFs in having a muscular layer surrounding the vacuole cells but the number of the cells is small, and the contents of the vacuole usually stains bluish or sometimes violet. The homogeneity of the contents also varies. It can be granular or homogenous. The diameters of the structures are ~100 µm and a duct leading to the outside can be observed. Melibe leonina also shows globular structures containing vacuole cells which stain bluish or do not stain at all. These structures lack a muscular layer and a duct leading to the outside (Figure 9D). In addition to these MDF-like structures, Melibe also possesses agglomerations of cells with a large nonstaining vacuole (Figure 6C). The size of these agglomerations comes close to that of real MDFs. The cells are loosely connected by connective tissue in an almost tissue-free notum. This unusual type of gland is listed with the MDFlike structures. Several species show larger globular structures sometimes even surrounded by muscle fibres and therefore resembling MDFs, but their general appearance differs. Plocamopherus ceylonicus even shows two different types, one with a duct leading to the outside and filled with small, rodlike structures (Figure 9A, arrow), and one type without a duct and composed of several globular subunits (Figure 9B). These subunits are composed of vacuoles of different sizes, the smaller ones filled with homogenously dark bluish stained contents, the larger being lighter in colour. These 233

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Table 3 Details of MDFs, when known, from literature or own studies. See notes on page 240.

MDFs present Sacoglossa Plakobranchus ocellatus van Hasselt, 1824 Elysia ornata (Swainson 1840) Cephalaspidea Newnesia antarctica Smith, 1902

Type

Maximum size (including layer), µm

Thickness of muscle layer, µm

Opening

Muscular structure connecting MDF to epidermis

References

3

500

Absent

Absent

Absent

Present work

2

?

?

?

?

Horgen et al. 2000

2

?

?

Absent

Absent

Present work

450

Absent

Absent

Present work

?

+

?

See figures for possible extrusions ?

?

1

700

Absent

With channellike exit

Absent

Valdés & Campillo 2000 Present work

?

+

?

?

?

Rudman 1995

?

+

?

?

?

Gosliner 1996

? ?

+ +

? ?

? ?

? ?

Gosliner 1996 Gosliner 1996

?

+

?

?

?

Gosliner 1996

?

+

?

?

?

Gosliner 1996

?

+

?

?

?

?

+

?

?

?

3

360

Absent

?

?

?

+

?

?

?

?

+

?

?

?

?

+

?

?

?

Absent

Absent

Absent

Absent

Absent

Gosliner & Behrens 1998 Gosliner & Behrens 1998 Present work, García-Gómez et al. 1991, Avila 1993, Avila & Durfort 1996 Gosliner & Behrens 2000 Gosliner & Behrens 1998 Gosliner & Behrens 1998 Ortea et al. 1996

Nudibranchia Doridoidea Cadlina laevis 1 (Linnaeus, 1767) Cadlina luarna (Marcus & Marcus, 1967) Cadlina marginata MacFarland, 1905 (= C. luteomarginata) Cadlinella hirsuta Rudman, 1995 Ceratosoma alleni Gosliner, 1996 Ceratosoma gracillimum Ceratosoma ingozi Gosliner, 1996 Ceratosoma tenue Abraham, 1876 Ceratosoma trilobatum (J.E. Gray, 1827) Chromodoris africana Eliot, 1904 Chromodoris annae Bergh, 1877 Chromodoris britoi (Ortea & Pérez, 1983)

Chromodoris buchananae Gosliner & Behrens, 2000 Chromodoris elisabethina Bergh, 1877 Chromodoris dianae Gosliner & Behrens, 1998 Chromodoris goslineri Ortea & Valdés, 1996

234

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DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS

Table 3 (continued) Details of MDFs, when known, from literature or own studies

MDFs present

Type

Maximum size (including layer), µm

Chromodoris hamiltoni Rudman, 1977 Chromodoris heatherae Gosliner, 1994 Chromodoris hintuanensis Gosliner & Behrens, 1998 Chromodoris joshi Gosliner & Behrens, 1998 Chromodoris kitae Gosliner, 1994 Chromodoris krohni (Vérany, 1846)

?

+

?

?

?

?

+

?

?

?

?

+

?

?

?

?

+

?

?

?

?

+

?

?

?

3

?

?

Absent

Absent

?

+

?

?

?

?

+

?

?

?

3

?

?

Absent

?

?

+

?

?

?

?

+

?

?

?

?

+

?

?

?

?

+

?

?

?

3

?

Absent

Absent

?

?

+

?

?

?

?

+

?

?

?

?

+

?

?

?

1

350

Absent

Whole vacuoles (see Figure 5A)

Absent

Chromodoris lochi Rudman, 1982 Chromodoris luteopunctata (Gantés, 1962) Chromodoris luteorosea (Rapp, 1827)

Chromodoris magnifica (Quoy & Gaimard, 1832) Chromodoris mandapamensis Valdés, Mollo & Ortea, 1999 Chromodoris michaeli Gosliner & Behrens, 1998 Chromodoris naiki Valdés, Mollo & Ortea, 1999 Chromodoris purpurea (Laurillard, 1831)

Chromodoris loboi Gosliner & Behrens, 1998 Chromodoris strigata Rudman, 1982 Chromodoris trimarginata (Winckworth, 1946) Chromodoris tumulifera Collingwood, 1881

Thickness of muscle layer, µm

Opening

Muscular structure connecting MDF to epidermis

235

References Gosliner & Behrens 1998 Gosliner 1994b Gosliner & Behrens 1998 Gosliner & Behrens 1998 Gosliner 1994b Present work, García-Gómez et al. 1991, Avila 1993 Gosliner & Behrens 1998 García-Gómez et al. 1991 Present work, García-Gómez et al. 1991, Avila 1993 Gosliner & Behrens 1998 Valdés et al. 1999

Gosliner & Behrens 1998 Valdés et al. 1999 Present work, García-Gómez et al. 1991, Avila 1993 Gosliner & Behrens 1998 Gosliner & Behrens 1998 Valdés et al. 1999 Present work

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HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA

Table 3 (continued) Details of MDFs, when known, from literature or own studies

MDFs present

Type

Maximum size (including layer), µm

Chromodoris westraliensis (O’Donoghue, 1924)

3

450

Chromodoris willani Rudman, 1982 Doriopsilla gemela Gosliner, Schaefer & Millen, 1999 Durvilledoris albofimbriae Rudman, 1995 Glossodoris atromarginata (Cuvier, 1804) Glossodoris aureola Rudman, 1995 Glossodoris edmundsi Cervera et al. 1989 Glossodoris pallida (Rüppert & Leuckart, 1828) Glossodoris rufomarginata (Bergh, 1890) Gymnodoris aurita (Gould, 1852)

?

+

Homogeno us layer (5–10) ?

1

60

1 kg dry weight (DW) m–2 y–1 (Bouchard & Lefeuvre 2000). Toward the end of the growth season, above-ground parts of many saltmarsh plants die back, and during storms or spring tides, these may be transported away (Figure 9). Export from salt marshes into nearby coastal habitats has been well known for decades (Teal 1962) and a large proportion of this export may be via the sea surface. It has been reported that dead or living parts of some saltmarsh plants are positively buoyant (Thiel & Gutow 2005b) but it is not well known how long these can persist at the sea surface. Dalby (1963) reported that seed-containing fragments of Salicornia pusilla may float for up to 3 months. Whole branches with fruits of the coastal plant Crambe maritima were found on beaches of the North Sea and it has been estimated that these may have come from source populations at least 7 km upcurrent (Cadée 2005). Most of these floating materials may be washed up in the flotsam in close vicinity of their sites of origin within the salt marsh: “Macrodetritus moved by tides from the production site in the low marsh accumulate in drift lines in the middle and high marshes, which act as sinks of organic matter” (Bouchard & Lefeuvre 2000). However, some of this dead organic matter may also be carried greater distances (Bouchard et al. 1998). Bart & Hartman (2003) suggested that during storm and hurricane events entire patches of saltmarsh vegetation can be eroded. Positively buoyant peat patches containing rhizomes may then be carried to other neighbouring salt marshes in a bay or estuary. Connectivity between populations of saltmarsh plants themselves is achieved via floating propagules of either vegetative (roots and rhizomes, e.g., Proffitt et al. 2003, Travis et al. 2004) or sexual origin (seeds and fruits, e.g., Huiskes et al. 1995). Potential dispersal distances of roots and rhizomes are not well known, but fruits and seeds have been reported to disperse at least over distances of 60 km via tidal currents (Koutstaal et al. 1987). Few studies are available on rafting 343

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Figure 8 Genetic relationships between populations of Zostera noltii from W Iberia. (A) Study sites along the Atlantic coast of Portugal and S Spain. (B) Neighbour-joining tree based on pairwise Reynold’s distances (using microsatellites). The northern populations and the southern populations are monophyletic and form sister clades. (C) Isolation by distance based on pairwise comparisons of genetic and geographic distance among eight populations. IBD pattern among all populations was significant (Mantel test, p < 0.016), but no significant IBD was found for the southern populations (p < 0.549), suggesting a high degree of connectivity between them. Figures modified after Diekmann et al. (2005).

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Figure 9 Dynamics on frequent rafting routes supported by saltmarsh vegetation. (A) Detached shoots, senescent plants or patches with rhizomes floating to the sea surface and that are dispersed by currents. (B) Plants of Spartina sp. during high tide with entangled seagrass shoots. (C) Annual pattern of biomass export from a salt marsh on the French Atlantic coast; after Bouchard & Lefeuvre (2000). (D) Proportion of macrofaunal groups found in larval collectors (L.C.) and on floating rafts in a restored salt marsh in California; after Moseman et al. (2004).

transport of organisms associated with saltmarsh plants, but it is known that gastropods climb up the stem of marsh grasses and diverse insects feed on and reproduce in saltmarsh plants. A diverse fauna inhabits the rhizome mats of salt marshes, and several recent studies indicate that saltmarsh plants and algae serve as dispersal vectors for these organisms within bay systems. In a restored salt marsh, Moseman et al. (2004) observed diverse organisms, including polychaetes, turbellarians, molluscs, crustaceans and insects arriving on algal rafts (Figure 9), and they concluded that rafting transport contributes large numbers of colonisers to salt marshes. Levin & Talley (2002) made similar observations at another restoration site: all initial colonisers arrived via rafting (on seagrasses, saltmarsh vegetation and macroalgae), and most of them included macrofauna with mobile adults and without planktonic larval stages (for example the amphipods Hyale frequens, Pontogeneia rostrata and Jassa falcata, the tanaid Leptochelia dubia, the gastropods Barleeia subtenuis and Cerithidea californica, and several annelids). Those authors also noticed abundant rafting dispersal in a neighbouring undisturbed salt marsh, emphasising that “rafting of macrofauna is also common in undisturbed settings”. They concluded that the high rates of recolonisation are partly made possible by the high degree of connectivity between saltmarsh patches within bay systems. 345

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Figure 10 (A) Adult of the beetle Agapanthia villosoviridescens (photo courtesy of Per H. Olsen). (B) Dry weight of the larvae of A. villosoviridescens collected in flotsam and in standing saltmarsh plants at different sites in the estuary; the large size of larvae found in down-estuary flotsam suggest up-estuary sources. (C) Cumulative emergence of larvae of A. villosoviridescens from flotsam, and from standing plants at the presumed site of origin (Soeftinge) and another site (Ellewoutsdijk); the similarity of emergence-pattern between down-estuary flotsam and up-estuary plants suggests up-estuary sources. (D) Sites in the Westerschelde estuary where larvae were collected in flotsam and in standing saltmarsh vegetation. Figures (B–D) modified after Hemminga et al. (1990).

Wilhelmsen (1999) revealed a high degree of connectivity between local populations of Littorina saxatilis and she suggested that dispersal may occur via floating marsh grass or seagrass shoots. Strong evidence for efficient dispersal of insects via saltmarsh vegetation comes from a study by Hemminga et al. (1990). Those authors collected large numbers of viable larvae of the beetle (Agapanthia villosoviridescens) in dead stems of Aster tripolium that had accumulated in flotsam of the Schelde Estuary (NL). Based on morphological evidence and of accompanying saltmarsh vegetation in flotsam, the authors concluded that these larvae had rafted to the collecting sites from upstream source populations (Figure 10). This transport mechanism appears to be important since adults of this beetle “rarely seem to fly”. Hemminga et al. (1990) also observed other species in the hollow stems and they suggested that “tidal transport of insects [via rafting] between isolated estuarine salt marshes is an actual process and probably is more common than is apparent until now”. Many insects overwinter as larval or pupal stages in senescent saltmarsh vegetation (Denno 1977, Denno et al. 1981), which during winter storms may become detached and dispersed with tidal currents, thereby contributing to connectivity between subpopulations within estuaries. In this 346

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context it appears interesting that Peterson et al. (2001) revealed strong gene flow between local populations in a predominantly flightless plant hopper (Tumidagena minuta), which lives under the layer of plant debris accumulating in the high salt marsh. Possibly, dispersal of this species is achieved when detritus in the upper marsh goes afloat during strong winter storms. Shallow-water macroalgal belt The intertidal belt and shallow subtidal waters of temperate regions in both hemispheres are colonised by lush populations of intermediate-sized macroalgae. Many of these algae possess gas-filled structures providing positive buoyancy to these species (e.g., Ascophyllum spp., Fucus spp., Sargassum spp.) (Thiel & Gutow 2005a). Thalli or whole individuals of these algae are frequently detached due to grazer-activity or wave-induced failure and may then float away. There are abundant reports of these algae encountered on sandy beaches (e.g., Stegenga & Mol 1983), yet surprisingly little is known about their arrival on rocky shores or in other subtidal habitats. Also, no data on quantity and direction of export fluxes of these intermediatesized algae are available. However, based on anecdotal accounts it appears safe to assume that much of the ungrazed annual production of the buoyant algae in these algal belts will be exported via the sea surface to surrounding areas or regions. As a result of their intermediate longevity these algae may be efficiently moved around within estuaries, lagoons or bays, but they may also be frequently exported from these systems (see also below). Dense patches of these algae have been reported from large marine systems such as the North Sea (Franke et al. 1999, Gutow & Franke 2003, Vandendriessche et al. 2006), the Irish Sea (Davenport & Rees 1993), the British Channel and the Baltic Sea (M. Thiel, personal observations), the Gulf of Maine (Locke & Corey 1989), the Strait of Juan de Fuca (Shaffer et al. 1995), and the Japan Sea (Segawa et al. 1964). Many species of these intermediate-sized algae are colonised by a diverse biota including mobile and sessile species (Mukai 1971, Norton & Benson 1983, Kitching 1987, Ingólfsson 1998, Fredriksen et al. 2005, Buschbaum et al. 2006). Mobile grazers such as isopods from the genus Idotea are commonly found on floating Fucus vesiculosus and Ascophyllum nodosum (Gutow 2003). In laboratory experiments, it could be shown that Idotea baltica rapidly consumes its floating substratum (Gutow & Franke 2003). Since this species is restricted to coastal areas, the author suggested that, after exploiting a patch of floating algae, these highly mobile isopods (see Orav-Kotta & Kotta 2004) may return to benthic populations or search for new floating patches (Gutow & Franke 2003). Thus, I. baltica appears to be capable of exploiting floating patches as food resources. Similar relationships can be expected for other mobile crustaceans such as palaemonid or hippolytid shrimp. Common decomposers of detached algae such as amphipods from the genus Orchestia or isopods from the genus Ligia have also been found on floating algae in estuaries (Wildish 1970). Juvenile stages of many fish species associate with floating algae, where they forage on associated rafters (e.g., Shaffer et al. 1995, Ingólfsson & Kristjánsson 2002). In addition to mobile species, many sessile organisms are found on these algae, including spirorbid polychaetes, hydrozoans, bryozoans and ascidians. Due to the small size of the holdfasts of these intermediate-sized algae, most organisms grow on their blades. The high abundance and intermediate longevity of these floating algae facilitate not only temporary exploitation of these ephemeral habitats, but also efficient dispersal of associated organisms within bays, and occasionally even between bays along the outer coast. Some indication for connectivity among populations, both within and between bays, on relatively small spatial scales comes from a study by Engelen et al. (2001) on floating algae. They suggested some connectivity between bays via rafting individuals but they also noted local differentiation (Figure 11). For two common epibionts on fucoid algae, rafting has also been inferred to contribute to population connectivity (for the nudibranch Adalaria proxima – Todd et al. 1998 and for the bryozoan Alcyonidium gelatinosum – Porter et al. 2002). Similarly, the gastropod Littorina saxatilis may also be dispersed on floating fucoids (Johannesson & Warmoes 1990). 347

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Figure 11 Genetic population structure of Sargassum polyceratium on the Caribbean island of Curaçao. (A) Neighbour-joining diagrams for pairwise genetic distances (using RAPD data) of populations from shallow water sites — two distinct clusters, one in the north and one in the south can be distinguished. (B) Typical current and wind patterns around Curaçao. Figures modified after Engelen et al. (2001).

Mangrove forests Mangroves produce a wide variety of detritus that is positively buoyant, including wood (Si et al. 2000) and leaves (e.g., Wehrtmann & Dittel 1990). While substantial research has been conducted on the fate of fallen leaves in mangrove forests (Lee 1999, Jennerjahn & Ittekkot 2002, Alongi et al. 2004), surprisingly little information is available on the amounts and characteristics of fallen wood: “Despite considerable research interest in the ecology of mangrove forests, there is a surprising paucity of information concerning the role of wood in these systems” (Romero et al. 2005). Leaves and small twigs become available every year with seasonal peaks at the end of the summer/fall (Mfilinge et al. 2005), while large pieces of wood only are supplied to the aquatic system following episodic events, such as hurricanes (Krauss et al. 2005). A large proportion of this detritus is exported to nearby coastal habitats (Odum & Heald 1975) as has been demonstrated by numerous studies on trophic links in mangrove systems (Marchand et al. 2003, Alongi et al. 2004), but little information is available about the transport mechanisms. Fallen leaves and twigs of many species are positively buoyant (see, e.g., photograph in Stieglitz & Ridd 2001) and they may locally be very abundant: “Remarkable concentrations of floating debris, especially of mangrove leaves, were at several tidal fronts” (Wehrtmann & Dittel 1990). In general, it appears safe to assume that leaves of most species have only a limited survival time (days) at the sea surface 348

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(see Kathiresan & Bingham 2001). Seeds of mangroves may have higher longevities, i.e., several weeks (Steinke & Ward 2003). No information is available about the buoyancy of mangrove wood and its longevity at the sea surface. This makes it difficult to estimate potential transport distances within estuaries and bays. Since mangrove leaves, twigs and seeds are not in contact with sea water before entering the rafting circuit, they may serve as rafts for terrestrial organisms. It is considered likely that terrestrial arthropods or their developmental stages, which are inquilines in leaves, leaf-stems, twigs or seeds (Feller & Mathis 1997), are dispersed within and between neighbouring mangrove forests, similar to what has been shown by Hemminga et al. (1990) for insects in saltmarsh vegetation (see above). Feller & McKee (1999) mentioned for the wood-boring beetle Elaphidion mimeticum, that “dispersal of this species from the mainland to the offshore mangrove islands probably occurred via rafting in wood”. Even though aerial parts of mangroves are only of limited value as dispersal vector to marine organisms, some highly mobile ephemeral rafters such as megalopae or juveniles of decapod crustaceans, and also peracarid crustaceans, are known to utilise them as transport vehicles (Wehrtmann & Dittel 1990). Parts of mangroves that are exposed to sea water before going afloat may be more important as substratum for potential marine rafters. For example, submerged aerial roots of the red mangrove Rhizophora mangle are colonised by a diverse biota, mostly composed of sessile suspension feeders (Bingham & Young 1995). These organisms may be transported to new sites, when roots break off. This is facilitated by boring organisms, such as teredinid bivalves or sphaeromatid isopods. In particular, isopod borers have been held responsible for breakage of mangrove roots, and subsequent loss of mangrove trees (Rehm & Humm 1973, Svavarsson et al. 2002). Thus, with their boring activity, isopods may indirectly facilitate dispersal of the biota growing on/in aerial roots of mangroves. Indeed, Brooks (2004) suggested that Sphaeroma terebrans may be dispersed with the roots of Rhizophora mangle. Detached roots may float for up to 2 months (Estevez 1978, cited in Brooks 2004) and thus they may be efficiently dispersed by tidal currents within mangrove forests and lagoons. There is some indication that population connectivity of Sphaeroma terebrans within enclosed bays is high. Baratti et al. (2005) observed little genetic variation among individuals collected within each of four sites in Kenya (two sites), Tanzania and Florida, but they revealed substantial differences between sites (Figure 12). They also reported a limited degree of connectivity between the East African populations, and they suggested occasional rafting dispersal with floating mangrove wood. Reid (2002) also mentioned that littorinid gastropods that inhabit mangrove fringes may be dispersed via rafting (possibly on floating wood). Local populations of boring isopods and other root biota appear not to be dispersal-limited, and their distribution within bays and lagoons may rather be influenced by abiotic factors such as temperature, salinity, tidal level or seston load (Brooks 2004). Dispersal dynamics on frequent rafting routes Supply of floating substrata in seagrass beds, salt marshes, macroalgal belts and in mangroves is highly predictable. In some of these environments, substrata are supplied continuously, but with some seasonal variation in abundance and size of floating items. Most of these substrata have a limited survival time at the sea surface (days), but occasionally they may float for several weeks. Longevity of substrata appears sufficient to guarantee efficient dispersal within estuaries, lagoons and bays. In these systems, organisms that already grow on these substrata at the moment of detachment or that are capable of holding onto them may become efficiently dispersed. Since many of the habitats discussed above intercept the sea surface at some time during the tidal cycle or generate layers with reduced flow above them (Dame et al. 2000), they are also very efficient in retaining floating substrata. Thus, rafting dispersal may be an important component of the population dynamics of 349

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Figure 12 Dynamics on frequent rafting routes supported by mangroves. (A) Detached roots, branches or leaves float at the sea surface and are dispersed by currents. (B) Dense meshwork of aerial roots of the red mangrove Rhizophora mangle (photo courtesy of Ingo Wehrtmann, Universidad de Costa Rica, Costa Rica). (C) Global distribution of the isopod Sphaeroma terebrans, which excavates burrows in aerial roots of R. mangle, and map of study sites along the coast of E Africa. (D) Haplotype minimum spanning network of partial sequence of mitochondrial cytochrome oxidase I gene from different populations of S. terebrans, size of ovals (haplotypes) and squares (haplotype with highest outgroup probability) represent the frequency of haplotypes; after Baratti et al. (2005).

organisms living in these habitats. Colonisation of habitat patches may proceed rapidly and via multiple immigration events. In dense subpopulations, emigration events may commonly occur, resulting in rapid spreading of individuals from local populations within estuaries, lagoons and bays, permitting efficient exploitation of resources. The realised geographic distribution of these species within bays will thus depend on environmental factors (both biotic and abiotic), rather than on dispersal supply as long as source populations persist within bays or estuaries (see also Wildish 1970). If subpopulations are effectively connected within a bay, but without input from local populations in adjacent bays, loss of genetic diversity could be expected (see Figure 6). Some indication for this comes from a study by Hoagland (1985) who observed absence of rare alleles in a small introduced population of the gastropod Crepidula fornicata in southern England. When input from neighbouring populations occurs, genetic diversity may increase. Dupont et al. (2003) suggested that jump-dispersal (in that case mediated by human transfer) between local populations in neighbouring bays may be responsible for the high genetic diversity observed in French populations. 350

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This indirectly confirms the expectation of high genetic diversity in local populations of rafters on frequent rafting routes that occasionally receive inputs from external populations (see Figure 6). Based on the high predictability of rafting opportunities, it can be hypothesised that some species may have evolved particular morphological and behavioural adaptations, allowing them to exploit the opportunities offered by these substrata. Mobile species able to cling efficiently to floating substrata and to swim rapidly in search of new rafts or benthic habitats appear to be preadapted to exploit opportunities for rafting dispersal. Seagrass- and algal-dwelling isopods from the genera Cleantis, Erichsonella and Idotea, amphipods and hippolytid shrimp seem to be the most likely candidates. They are frequently found on floating seagrass blades (M. Thiel, personal observation), but presently it is not known whether these are accidental rafters or whether, under certain conditions, some individuals actively seek out floating blades in order to be transported to other parts of a seagrass bed or even to neighbouring habitat patches. Occasionally floating items may also be flushed out of estuaries or bays. Baratti et al. (2005) suggested that strong ebbing currents could eject floating mangrove parts into coastal waters, where they may then be transported over greater distances. Snyder & Gooch (1973) mentioned that (rafting) “snails [Littorina saxatilis] may occasionally be swept offshore during violent storms and be deposited at new sites”. Hemminga et al. (1990) also remarked that saltmarsh vegetation may occasionally leave estuaries. Once carried out of estuaries, lagoons or bay systems into coastal offshore waters, the probability of successful transport to suitable habitats will decrease substantially, because in addition to estuarine shores (seagrasses, salt marshes, macroalgal belt, mangrove forests), many of these floating substrata may end up on inhospitable shores (sandy beaches, exposed rocky shores, etc.). Dispersal dynamics of floating substrata from frequent rafting routes that are carried into offshore waters are expected to be more similar to those on intermittent rafting routes. Local populations of organisms rafting on intermediate-sized algae and on floating mangrove debris may thus exhibit connectivity that is characteristic of the frequent rafting routes within bays, but the metapopulation connectivity of these species outside of bays may resemble that typical for organisms dispersed on intermittent rafting routes.

Intermittent natural rafting routes Regular supply of floating substrata on intermittent rafting routes As already outlined in the previous section there may exist substantial overlap between frequent and intermittent routes. The main difference between them is the spatial scale at which they occur. While frequent rafting routes occur within bays or adjacent or continuous patches of habitat, intermittent routes connect different bays or non-adjacent patches of habitat. Since intermittent routes encompass a longer voyage, they present a more selective filter for species, and thus, for many species the likelihood of successful rafting may be lower than on frequent rafting routes. In coastal offshore waters, floating substrata may be available on a regular basis, but abundance and floating direction can vary substantially between years. Substrata are supplied from coastal sources (e.g., kelp forests or rivers). These floating substrata are dispersed within alongshore coastal currents or with major oceanic currents. Strong winds may also influence the floating direction and velocity of these substrata (Harrold & Lisin 1989, Johansen 1999). In the case of giant kelps, these are already inhabited by a wide variety of species before becoming detached, while wood may or may not be colonised when entering offshore waters, depending on its origin and residence time in nearshore coastal waters. Both substrata have intermediate longevities, and can thus travel over intermediate distances throughout biogeographic regions. In addition to the giant kelps, intermediate-sized macroalgae are available on a regular basis in coastal waters, and these can also transport organisms within offshore currents (see above). Many observations of these substrata in coastal 351

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currents and in the open ocean are available (for summary see Thiel & Gutow 2005a), but surprisingly little is known about the local populations connected via these substrata. Given that floating substrata are common on intermittent rafting routes, it can be predicted that these routes may lead to high-to-intermediate levels of population connectivity. Since distances connected by intermittent routes are relatively large (100–5000 km), not all local populations will be continuously connected via this rafting route. Small local populations may be temporarily isolated, possibly resulting in founder effects. Also, as a consequence of comparatively large distances over which intermittent rafting routes are effective, IBD may increasingly gain in importance if hydrographic conditions regularly result in the same rafting trajectory. Under these conditions, the relatedness of neighbouring local populations will depend to a high degree on current velocity and directions. Stepping-stone dispersal is expected to be a predominant pattern on intermittent rafting routes that have a fixed route. This usually leads to colonisation of neighbouring local populations, and thus, distant local populations may only be connected via intermediate local populations (Figure 13). However, since floating substrata on intermittent rafting routes have a A Intermittent rafting route; alongshore convergent currents

B

Intermediate connectivity: Disrupted IBD

Intermediate connectivity: Disrupted IBD

C

Intermittent rafting route; alongshore divergent currents

D

Intermittent rafting route; alongshore directional currents

Intermediate connectivity: Stepping-stone with IBD

Intermittent rafting route; alongshore directional current

Intermediate connectivity: Leapfrog dispersal, no IBD

Figure 13 Scheme showing four possible scenarios on intermittent rafting routes and the expected genetic consequences. (A) shows an intermittent rafting route with convergent currents, while (B) shows a route with divergent currents; in both cases the alongshore populations are not expected to show an IBD pattern because not all local populations are connected by currents. (C) shows an intermittent rafting route with consistent alongshore currents resulting in local populations being connected in a stepping-stone manner and in an IBD pattern of genetic differentiation. (D) shows an intermittent rafting route with consistent alongshore currents where rafters may occasionally be transported over long distances jumping over adjacent local populations, which results in lack of IBD.

352

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relatively high longevity, gene flow in an alongshore direction may not occur in a stepping-stone fashion (or other dispersal/colonisation mechanisms that may ultimately lead to IBD), but rather in a leapfrog fashion where propagules may leap over immediately neighbouring populations and immigrate into distant populations (Figure 13). In these situations, the pattern of genetic structure of the metapopulation should not be IBD. It is important to characterise this specific form of jumpdispersal, because a particular pattern in genetic population structure might result from leapfrog dispersal, namely that distant populations are more similar than adjacent local populations. Leapfrog dispersal may occur at all scales, because there exists a high variability in individual dispersal distances among rafters. Genetic diversity of many species connected via intermittent rafting routes can be expected to be structured as a metapopulation with varying degrees of connectivity among local populations. Local populations will be more or less both temporarily isolated and connected, such that in some cases gene flow obscures the effects of genetic drift (either in the form of bottlenecks or founder effects), which would be reflected in a low genetic differentiation among local populations. At the other extreme, intermittent routes may sometimes act as a strong filter that results in a lower probability of successful colonisation by rafters, but that is still frequent enough to prevent speciation. In these cases, genetic differentiation among local populations will be higher. Examples of intermittent rafting routes Kelp forests In temperate regions of the Pacific and of the Southern Ocean, giant kelps grow between ca latitudes 30˚ and 60˚ in both hemispheres (Steneck et al. 2002). These kelp forests contain many species that are positively buoyant thanks to gas-filled structures. Detachment of these kelps may be caused by strong wave action (Dayton & Tegner 1984), by high grazer activity (e.g., Tegner et al. 1995), or a combination of both (Barrales & Lobban 1975). Following detachment, kelp with floating structures rise to the sea surface (Kingsford & Choat 1985, Kingsford 1992) where they are transported with major currents or pushed by prevailing winds (Harrold & Lisin 1989). Some authors reported that the abundances of floating kelp increased during late summer/ early fall (e.g., Kingsford 1992), while other studies revealed no clear seasonal trend (Hobday 2000b). Kelp forests grow in nearshore coastal habitats, and consequently detached individuals may be exported immediately onto nearby beaches where they constitute an important subsidy to the community of sandy beach detritivores (Orr et al. 2005). Kelp species with limited buoyancy or those that have lost buoyancy due to degradation processes may also sink to the sea floor, where they accumulate in submarine canyons constituting an important food source for benthic organisms (Vetter & Dayton 1999). However, abundant reports of floating kelps at far distances from the nearest source populations also indicate that they can potentially travel substantial distances while afloat (Helmuth et al. 1994, Kingsford 1995, Hobday 2000b, Smith 2002, Macaya et al. 2005). During offshore voyages, these kelps may carry a diverse community of associated organisms, which, upon landfall, may colonise benthic habitats. Large kelp from the genera Macrocystis, Nereocystis, Pelagophycus and Durvillaea possess a large and structurally complex holdfast, which is inhabited by a wide diversity of organisms (e.g., Ojeda & Santelices 1984, Smith & Simpson 1995, Adami & Gordillo 1999, Thiel & Vásquez 2000). Depending on their biology and on the structure of the holdfast, these organisms may persist in the holdfast after detachment. For example, many inhabitants of holdfasts of Macrocystis pyrifera survived for several months in detached holdfasts (Edgar 1987, Vásquez 1993). Connectivity between neighbouring kelp forests is hypothesised to be high. Some indication for this comes from genetic studies on positively buoyant kelp species. For the elk kelp Pelagophycus porra, Miller et al. (2000) revealed that individuals from several Channel Islands off southern California were too similar to represent different species, but they observed a trend of isolation. 353

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Figure 14 Dynamics on intermittent rafting routes supported by giant kelps. (A) Detached blades, branches or whole individuals float at the sea surface and are dispersed by currents. (B) Floating giant kelp Macrocystis pyrifera along the SE Pacific coast of Chile. (C) Phylogram based on nuclear ITS2 sequences of populations of M. pyrifera, indicating the close relationship of populations from the southern and northern hemisphere; after Coyer et al. (2001).

Interestingly, in a subsequent ‘distance network analysis’ some individuals from different islands clustered together, and even though they observed floating sporophytes, the authors did not mention rafting dispersal as a potential explanation. Using rDNA, Coyer et al. (2001) examined the genetic relatedness among four putative species of Macrocystis (Figure 14), and their results led them to suggest that “Macrocystis may be a monospecific genus (M. pyrifera)”. They furthermore noted high “intra-individual variability” in the samples from the northern hemisphere (in particular those from the Channel Islands). Inferring rafting dispersal of fertile sporophytes, they hypothesised that “southern genotypes ‘hybridize’ with northern genotypes in intermediate areas such as Santa Catalina Island” (Coyer et al. 2001). This scenario would fit the hypothesised gene flow on regular rafting routes with alongshore convergent currents (Figure 13). Another indication of efficient dispersal via floating kelps comes from the wide geographic distribution of some common kelp inhabitants. Despite lacking a pelagic dispersal stage, the kelpboring isopod Limnoria chilensis is found in kelp holdfasts extending over a wide geographic range of >4000 km between 20 and 55˚S (Thiel 2003a). Other kelp inhabitants with direct development also have wide geographic distributions (Knight-Jones & Knight-Jones 1984, Helmuth et al. 1994). This evidence for rafting dispersal admittedly is circumstantial, and it is emphasised that future studies on the population connectivity of organisms associated with giant kelp are highly desirable. Intermediate-sized algae (Ascophyllum spp., Fucus spp., Sargassum spp.) are also frequently found in coastal currents (Thiel & Gutow 2005a), which they may have reached after detachment from sheltered bays or from outer-coast rocky shores. These algae can also contribute to population 354

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connectivity within these systems via effective transport of organisms without planktonic larval stages (e.g., Littorina sitkana, Kyle & Boulding 2000; Amphipholis squamata, Sponer & Roy 2002; Nucella lapillus, Colson & Hughes 2004). The relatively high abundance of floating giant kelp in temperate coastal currents, and their intermediate longevity of several months (Thiel & Gutow 2005a), suggest that these are efficient dispersal vectors within biogeographic regions. Recolonisation of disturbed patches may proceed relatively slowly over several years. In particular toward the limits of the distributional ranges, where extinctions can occur relatively frequently, impoverished genetic diversity can be expected. Floating trees Rivers regularly transport large amounts of floating wood to the sea. In the northern hemisphere, north of ca 60°N, this occurs every year in the spring following snow melt (Maser & Sedell 1994, Johansen 1999). At low latitudes, around the equator, wood becomes available on a less regular basis, with relatively high interannual variation in abundances (Solana-Sansores 2001, Castro et al. 2002). If floating wood is immediately pushed into offshore waters, colonisation by marine organisms will occur during the journey (i.e., in the pelagic environment without direct contact with benthic communities). Wood may also be retained in or close to benthic nearshore communities (e.g., in salt marshes, kelp forests or in mangrove systems), and during this time become colonised by common coastal organisms. While wood may serve as the dispersal vehicle for many different marine organisms, its utility for terrestrial organisms is relatively limited. Only species which are not directly exposed to saltwater (e.g., in self-excavated burrows), or which resist immersion in saltwater (e.g., dormant stages), may survive extensive trips on floating wood. After reaching offshore waters, floating wood is presumed to follow a similar fate as kelp rafts. A large proportion of the total pool of floating wood may be thrown onto beaches during onshore storms, while the other fraction will sink to the sea floor where they sustain a diverse community of woodboring organisms (Distel et al. 2000). There are surprisingly few studies on population connectivity via floating wood, despite the fact that this substratum is relatively abundant in some regions. In the Arctic Ocean, the distribution of some coastal plant species is assumed to be the result of seed dispersal via rafting (Johansen & Hytteborn 2001) (Figure 15). Baratti et al. (2005) inferred limited exchange between local bay populations of the boring isopod Sphaeroma terebrans along the outer East African coast (see Figure 12). They suggested that isopod-bearing roots may occasionally be flushed out of bays into offshore waters. Lapègue et al. (2002) demonstrated close genetic relationships between mangrove oysters from West Africa and eastern South America and they suggested rafting (possibly on mangrove wood?) (Figure 15). In the Caribbean, there is an indication that population connectivity between island population of lizards may be achieved via rafting (Calsbeek & Smith 2003). Wood may be the primary rafting substratum for lizards as underlined by a direct observation of a group of iguanas that arrived on the Caribbean island Anguilla on a tree-raft (Censky et al. 1998). Insects were found on driftwood stranded on sandy beaches (Wheeler 1916) or floating in the sea (Heatwole & Levins 1972). Several other authors had suggested wood as dispersal substratum connecting insect populations of island groups in archipelagos and between islands off continental coasts (Abe 1984, Niedbala 1998, Coulson et al. 2002). Most of these observations are from subtropical and tropical areas, underlining the importance of floating wood as connecting vector in these regions. Dispersal dynamics on intermittent rafting routes While floating items (kelp and wood) can be underway in large quantities on intermittent rafting routes, the strength of the connectivity between local populations in general is lower than on frequent routes, primarily because transport distances are farther and local populations are more dispersed, diminishing the probability of landfall in suitable habitats. Nevertheless, fast recolonisation 355

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Figure 15 Intermittent rafting routes supported by floating trees. (A) Distribution pattern of Potentilla stipularis from Arctic coasts and predominant current patterns in the Arctic Ocean; modified after Johansen & Hytteborn (2001). (B) Distribution of 16S mtDNA haplotypes of mangrove oysters from W Africa and eastern S America and predominant current patterns in the S Atlantic; modified after Lapègue et al. (2002).

of unpopulated areas (Colson & Hughes 2004), and high genetic relatedness among distant local populations of some species, show that rafting dispersal on these intermittent rafting routes can be effective. Gene flow can be directional when alongshore currents are highly persistent, but there are also apparent examples of gene flow in variable directions. Dispersal via rafting often seems not to proceed in a stepping-stone fashion, commonly resulting in lack of IBD. A pattern of leapfrog migration, where travelling individuals are passing adjacent local populations and reach distant locations, appears to be a recurrent observation on intermittent rafting routes, irrespective of the floating substratum. The first example for this was found in one of the earliest studies on the genetic

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Figure 16 Relationships between local populations of an intertidal gastropod and a saltmarsh plant, assumed to being dispersed along intermittent rafting routes. (A) Sampling sites of local populations of the gastropod Nucella lapillus in SW England, and genetic cluster membership (based on microsatellites) of individuals collected at each site; the two most distant populations (1 and 10) show strongest similarities; modified after Colson & Hughes (2004). (B) Sampling sites of Elymus athericus from salt marshes on the SE coasts of the North Sea, and pairwise FST (based on microsatellites) plotted against geographic distance showing IBD pattern for the sampled populations; the local population from Helmsand (HS) is as closely related to a distant population (Sch) as to two adjacent populations (WH and SNK); modified after Bockelmann et al. (2003).

population structure of a marine invertebrate, the intertidal snail Littorina saxatilis (Snyder & Gooch 1973). These authors observed that “significant population differentiation may occur over distances of as little as 2 km, while widely separated populations may be nearly identical”. Colson & Hughes (2004) reported a similar pattern for local populations of Nucella lapillus: “The similarity between SW1 (St Agnes in North Cornwall) and SW10 (Stoke Beach in South Devon) is remarkable, considering the geographical distance between the two populations”, and they suggested “that the major dispersal routes involve relatively long-distance exchanges between open sea sites, bypassing Plymouth Sound” (Figure 16). In a study on the genetic population structure of the saltmarsh plant Elymus athericus, Bockelmann et al. (2003) also observed that distant populations were more similar than immediately adjacent populations: “Surprisingly, the Helmsand [HS] population was more similar to the populations on Schiermonikoog [Sch], although it is situated in a clayey mainland marsh in the northeastern Wadden Sea such as Sönke-Nissen-Koog Vorland [SNK] and Westerhever [WH]” (Figure 16). For the seagrass Thalassia testudinum, Waycott & Barnes (2001) revealed high levels

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of gene flow over distances of >2500 km (between Panama and Bermuda), and they suggested long-distance movements of vegetative fragments (possibly via rafting) as the principal explanation for the same clone being present in Panama and at Bermuda. Indication for the high floating potential of T. testudinum also comes from the finding of fragments of this seagrass in the deep sea off the Caribbean coasts (Wolff 1979), even though Flindt et al. (2004) assigned this species a low floating potential. It is suggested that many of these cases could be the result of leapfrog dispersal, where travellers jumped over long distances, leaving nearby populations out of the loop. For several rafting species, though, there is an indication of decreasing genetic diversity toward the limits of their biogeographic distribution (Marko 2004, 2005), suggesting that dispersal may occur along a chain of stepping stones. The reasons for decreasing genetic diversity toward range limits are primarily four-fold, namely (i) lack of suitable dispersal opportunities, (ii) limited propagule production, (iii) rapid range extension via few founding individuals or (iv) differential natural selection, which permits survival of different genotypes in source and sink regions. These factors may act in combination or separately — if they act in unison, their impacts might be enhanced. Toward the down-current end of intermittent rafting routes, dispersal may taper out and the frequency of events may take on a sporadic character similar to that on episodic rafting routes (see below). Based on global patterns of substratum supply, several intermittent rafting routes can be identified (Figure 17). Important intermittent rafting routes are known in the boundary currents of the Pacific, on the coasts of the North Atlantic, probably in the boundary currents of the South Atlantic (little is known from these regions), around southern New Zealand, also along the coasts around the equator, but at lower frequency than on the other intermittent rafting routes (Figure 17). In some of these regions (e.g., in the Humboldt and California Currents) during ENSO events, large-scale regional extinctions may occur. Rafting can contribute to a rapid recolonisation after such events, albeit possibly with few colonisers resulting in low genetic diversity (for algae see Martínez et al. 2003, for invertebrates Marko 2004).

Figure 17 Global distribution of important intermittent (shaded areas) and episodic (dotted lines) rafting routes. Regions with high abundances of floating wood and floating macroalgae indicated by dark and light shading, respectively.

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Episodic natural rafting routes Sporadic supply of floating substrata on episodic rafting routes In many regions of the world, for most of the time floating items may be virtually absent on the sea surface. However, after certain events, large numbers of these items suddenly become available as rafting substrata. This is, for example, the case with volcanic pumice, which may be supplied in large quantities after volcanic eruptions (Sutherland 1965; Jokiel 1989, 1990a; Bryan et al. 2004). Similarly, after cyclones, flood events or tsunamis enormous quantities of terrestrial debris may reach the oceans (Carey et al. 2001). Following these events, huge armadas of floating substrata may be transported with the predominant current systems, offering abundant rafting opportunities for potential travellers. Many of the substrata that become available episodically have very high longevities since they are either of abiotic origin (volcanic pumice) or consist of inorganic materials (skeletons) that are resistant to decay processes. Also terrestrial debris (e.g., large trees or processed wood) may survive for a relatively long time at the sea surface. Consequently, many of the floating items that are supplied sporadically may be transported over relatively large distances. Due to their origin either in terrestrial environments or in the open ocean, most of these substrata will only be colonised after starting their journey at the sea surface. The frequencies and localities at which these substrata are supplied to the ocean are difficult to predict. In general, volcanic pumice is most common in regions with high volcanic activity (e.g., the Pacific Ocean and the Mediterranean). Important volcanic eruptions, during which large quantities of volcanic pumice are released, appear to occur on a timescale of the order of several decades or centuries. For example surface eruptions were recorded in 1883 in Krakatau (Thornton 1997, Jokiel & Cox 2003) and in 1952 on San Benedicto (Richards 1958). Underwater eruptions producing buoyant pumice appear to take place over similar timescales (Sutherland 1965, Frick & Kent 1984, Fushimi et al. 1991, Bryan et al. 2004), in particular in the Pacific Ocean. Throughout a region with high tectonic activity, tsunamis may also wash terrestrial debris into the sea along wide stretches of impacted coastlines. Along the Pacific Rim, tsunami events are recorded to occur at a frequency of tens to hundreds of years (Witter et al. 2001, Pinegina et al. 2003, Kulikov et al. 2005). Similar frequencies are reported from other active margins (e.g., in parts of the Mediterranean (Altinok & Ersoy 2000)). In the tropics, large quantities of terrestrial debris may also be flushed out to sea after passage of hurricanes and typhoons. These tropical cyclones recur each year (e.g., Chan & Liu 2004), but their pathways and the input sites of terrestrial debris are highly unpredictable (Landsea et al. 1996, Weber 2005). Their frequency of occurrence in a given locality may be on the order of decades or centuries. Buoyant skeletal materials of marine organisms (floating corals, cephalopod shells, egg cases) only become available episodically, but then may be very abundant (Kornicker & Squires 1962, DeVantier 1992, Cadée 2002). In addition to these sporadically supplied substrata, some of the regularly available items such as floating macroalgae or wood may occasionally also travel on episodic rafting routes (e.g., during particular climatic or oceanographic events such as ENSO). In general, the temporal pattern of travel opportunities on these episodic rafting routes depends on the frequency of events that supply floating substrata. The unpredictability of most of these events makes it difficult (in many cases impossible) to provide estimates of the time intervals between subsequent rafting episodes. However, despite these uncertainties some simple statements can be made. In most cases, episodic events occur at intervals of many years, often decades or even centuries. It can thus be safely stated that the generation times of most small, coastal or terrestrial organisms are substantially shorter than the time intervals between supply events. Consequently, individuals supplying propagules to a given rafting episode will be descendents of several generations 359

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of residents that arrived after previous rafting events. In contrast, in clonal organisms, generation times may be of a similar magnitude as the intervals between rafting episodes. Individuals that established after one episode may be the same ones providing propagules for a subsequent rafting episode. As a consequence of the relationships between generation time and dispersal events, small sexually reproducing species with short lifetimes may reproduce over many generations without any (or with very little) exchange via rafting. During these time periods, dispersal will depend primarily on autonomous dispersal capabilities of organisms. This may lead to small effective population sizes of these organisms (i.e., on islands or in relatively isolated bays), with a high likelihood of founder effects to occur. In general, the degree of isolation of local populations will be negatively correlated with the potential for autonomous dispersal of a species (unless the episodic event has transported colonists into an area with frequent or intermittent rafting routes). Species with direct development can be expected to be most affected by periods of isolation of local populations. Interestingly, once rafting opportunities arise, some of these species are particularly well adapted for LDD and successful colonisation of new habitats (Thiel & Gutow 2005b). As a result of relatively long periods of isolation, local populations may diverge or even go extinct. Consequently, organisms that are transported during episodic rafting events may arrive in areas where conspecifics have experienced substantial genetic changes or are completely absent. Even when some degree of divergence has occurred or the new colonisers come into secondary contact with incipient species that derived from a common ancestral lineage, hybridisation may take place. If genetic changes have not yet led to reproductive barriers, genetic diversity of the metapopulation may reach high levels. In contrast, if allopatric evolution has led to reproductive isolation or if conspecifics are absent, founding populations may become established as a new species to the area. The genetic diversity of these local populations will depend on their history of isolation and the number and gene pool of arriving individuals. Since founding populations of direct developers on episodic rafting routes usually are small, genetic diversity of these may be relatively low. Thus, the dispersal dynamics on episodic rafting routes may lead to contrasting scenarios in the population biology of sexually reproducing organisms with short generation times. Genetic diversity in local populations may either show high or low levels, depending on whether arriving individuals can interbreed with local residents or not (Figure 18). In general, it can be predicted that the evolutionary consequences of episodic rafting routes depend on the relationship between generation times of rafting organisms and the time interval between subsequent rafting episodes. Examples of episodic rafting routes Volcanic pumice During volcanic eruptions enormous quantities of positively buoyant pumice can be released (e.g., Sutherland 1965, Jokiel 1990a, Bryan et al. 2004). Pieces of pumice usually are relatively small (several millimetres in diameter), but may occasionally be larger, reaching fist size — even pieces of >0.5 m diameter have been reported (Jokiel & Cox 2003). Pumice that is supplied to the sea may originate from island volcanoes (Richards 1958, Thornton 1997), or also from eruptions of underwater volcanoes (e.g., Coombs & Landis 1966, Fushimi et al. 1991, Bryan et al. 2004). Pumice pieces can float for many months and even years before disintegrating or washing ashore. During this time, the pumice and rafting organisms may be distributed throughout all major ocean basins (Frick & Kent 1984, Jokiel & Cox 2003, Bryan et al. 2004) (Figure 19). Diverse marine organisms are known to be transported with volcanic pumice. Algae, sponges, corals, polychaetes and bivalves have been found growing on volcanic pumice (Jokiel 1984, 1989; Bryan et al. 2004). How these organisms colonise the floating pumice in the first place is not well known. Pumice, as most other floating substrata on episodic rafting routes, enters the sea in a clean 360

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A

B

Episodic rafting route; singular dispersal event

Episodic rafting route; repeated dispersal events One source region

Founder effect: reduced genetic diversity

High population connectivity: similar genetic diversity

C Episodic rafting route; repeated dispersal events

D

Episodic rafting route; historic dispersal events

Multiple source regions

Multiple source regions

Mya Kya

High population connectivity: higher genetic diversity

No connectivity: allopatric speciation

Figure 18 Scheme showing four possible scenarios on episodic rafting routes and the expected genetic and biogeographic consequences. (A) showing a local island population arising from a singular dispersal event, where founder effects lead to a strong reduction in genetic diversity in the sink population. (B) showing a local island population supported by repeated dispersal events from a particular source region, resulting in close similarity between source and sink populations. (C) showing a local population supported by repeated dispersal events from several source regions, resulting in a high genetic diversity in the sink population. (D) showing a situation with several historic dispersal events, where local populations in the sink region have diverged significantly after the first dispersal event and could not anymore interbreed with subsequent colonists, leading to the establishment of two different species in the sink region.

state. Thus, it is most likely that pumice is colonised while floating, probably via planktonic (larval) stages. Many corals found on pumice have planktonic larval stages (Jokiel 1989), which is also true for other organisms reported from pumice, such as, for example, bivalves or stalked barnacles. In a laboratory experiment, Jokiel & Cox (2003) showed that similar numbers of planula larvae of Pocillopora damicornis settled and developed into juvenile colonies on volcanic pumice as on calcareous rock. They emphasised that P. damicornis produces larvae throughout the year, potentially permitting continuous colonisation of floating pumice. Bryan et al. (2004) remarked on the temporal coincidence between a pumice supply event and a spawning event: “It is noteworthy that the eruption and generation of the pumice rafts in this instance just preceded late spring coral spawning events in the southwest Pacific”. The necessity for close temporal overlap between pumice availability and propagule supply in a given locality enhances the sporadic character of dispersal on these episodic rafting routes. Several studies provide indication that volcanic pumice may serve as a dispersal vector with the potential of connecting distant populations. Strongest evidence comes from the studies by Jokiel 361

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Figure 19 Origins of volcanic pumice found on beaches on Hawaii and Christmas islands, and major oceanographic currents assumed to transport floating pumice from the different source regions; modified after Jokiel & Cox 2003. Shadings in map indicate sources of origin shown in the pie diagrams.

(1984, 1989, 1990a,b), who sampled volcanic pumice throughout the equatorial Pacific. His studies revealed that some species (e.g., P. damicornis) are frequently dispersed via pumice (Jokiel 1984, 1990b), though he remarked that organic substrata such as wood and seeds might be “far more important than pumice rafts in establishment of new populations of corals”, because rafting colonies are easily shed from these organic substrata when scratching over the reef (Jokiel 1989). Regardless of the floating substratum, rafting appears to be an important dispersal mechanism for some coral species. Observations of rafted colonies can be compared with studies on the geographic distribution or genetic diversity of these corals. Pocillopora damicornis is distributed throughout the tropical Pacific and Indic oceans and there is relatively good indication that distant populations may be episodically connected (e.g., during El Niño events) (Glynn & Ault 2000). However, populations from the East Pacific are spawners whereas those from the West Pacific are brooders (Glynn & Ault 2000), suggesting that connectivity between distant populations could be limited and might already have led to cryptic allopatric speciation. Ayre & Hughes (2004) revealed gene flow over large distances for P. damicornis and other corals along the Great Barrier Reef, but they did not specify whether dispersal might be achieved via larvae or via rafting. They did, however, emphasise that genetic exchange between distant populations is a highly episodic event: “Long-distance dispersal by corals to geographically isolated reefs cannot be achieved incrementally and is likely to be very rare” (Ayre & Hughes 2004). Interestingly, for this region, several reports of pumice-rafted

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Figure 20 (A) A small colony of the coral Pocillopora damicornis, growing on an algae-covered piece of volcanic pumice (photo courtesy of Scott Bryan, Yale University, U.S.) (diameter of coin is 16 mm), and (B) map of the SW Pacific indicating the inferred rafting routes of floating pumice originating from an eruption in the Tonga-Kermadec arc; modified after Bryan et al. (2004). (C) Estimates of gene flow (Nm) for two coral species from the Great Barrier Reef, one of which (P. damicornis) is very commonly reported as a rafter on volcanic pumice; modified after Ayre & Hughes (2004).

corals (including P. damicornis, Seriatopora sp. and Styllophora sp.) have been published (Jokiel 1990b, Bryan et al. 2004), suggesting that gene flow could indeed be achieved via rafting of adult colonies (Figure 20). Even though Ayre & Hughes (2004) do not discuss rafting, their results of gene flow on different spatial scales closely matches the predictions for processes on episodic rafting routes made above: “While long-distance gene flow over multiple generations is sufficient to limit genetic differentiation along the length of the Great Barrier Reef, most recruitment by corals on ecological time frames is decidedly local”. Results from a study by Wörheide et al. 2002 reported similar scales of connectivity for the tropical sponge Leucetta ‘chagosensis’ (Figure 21). They suggested that “small-distance dispersal was involved in the range expansion of clade 3–1, whereas some long-distance movements may be inferred for clade 3–4”, but they did not mention how LDD was achieved (possibly via pumice?). Little is known about dispersal and population connectivity via floating pumice for other organisms. This probably is due to the fact, that dispersal events are rare and that many other organisms (e.g., algae or bivalves) may quickly fall off pumice pieces after stranding (Jokiel 1990a). Ó Foighil et al. (1999) reported the presence of Ostrea chilensis in New Zealand and in Chile separated by >5000 km of open ocean (Figure 21). Since this species features direct development,

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Figure 21 (A) Distribution of the principal clades revealed for the tropical sponge Leucetta ‘chagosensis’ throughout its distribution range in the Indo-Pacific, and (B) distribution of the two clades found on the Great Barrier Reef; modified after Wörheide et al. (2002). (C) Unrooted phylogram based on mtDNA Cytochrome Oxidase I sequences depicting relationships between three populations of Ostrea chilensis (two from New Zealand and one from Chile) and two other species of the genus, and map of the Southern Ocean indicating the current direction of the West Wind Drift; modified after Ó Foighil et al. (1999).

these authors suggested that the trans-Pacific distribution pattern of O. chilensis may be the result of pumice-rafting. Empirical evidence for this transport mechanism and for continuing gene flow between New Zealand and Chilean populations, however, is not available at present. Terrestrial debris (after flood events, cyclones or tsunamis) Supply frequencies of terrestrial debris are similar to that of volcanic pumice. However, terrestrial debris supplied during episodic events comprises a heterogeneous assemblage of different substrata, from fragments of annual plants to entire trees. While it is well known that large amounts of floating substrata are travelling in adjacent seas after these events, little is known about the quantities and temporal dynamics. Tropical cyclones occur every year in the western parts of the central Pacific and the central Atlantic, but storm tracks vary substantially among years. A synthesis of the data provided by Landsea et al. (1996) shows that the hitpoints of hurricanes (where hurricane tracks and shorelines cross) vary substantially between years (Figure 22). Consequently, dispersal export from particular localities (e.g., islands) via terrestrial debris will occur only episodically. Storm and rain events were identified as main causes for interannual variation in abundance of floating terrestrial debris (Heatwole & Levins 1972, Zarate-Villafranco & Ortega-García 2000).

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Figure 22 Tracks of intense hurricanes in the W Atlantic over the eight-year period 1987–1995, showing that annual sites of hurricane landfall (star symbols) (and subsequent production of sporadic rafting opportunities) are spread throughout the region; modified after Landsea et al. (1996).

The importance of hurricane and storm events for episodic appearance of rafting opportunities is well known. For example, Simberloff & Wilson (1969), who studied the colonisation patterns on small mangrove islands in Florida Bay, noted that rafting dispersal may usually be of minor importance, because “except during hurricanes, there is very little floating debris”. In general, these events appear to have particular importance in the tropics where flood events, cyclones and tsunamis are most effective in transporting terrestrial debris to the sea. In the case of cyclone-related supply this is explainable by the fact that these phenomena occur mainly in the tropics. In the case of flood events and tsunamis these may achieve particular significance in the tropics due to the concentration of (a) many large and unregulated rivers in these areas, and (b) low-lying coral islands with little protection against tsunami or cyclone waves. Organisms found on this debris include terrestrial species such as insects and reptiles (Wheeler 1916, Heatwole & Levins 1972, Censky et al. 1998), but also marine organisms. Due to the singularity of events, little is known about connectivity between local populations via rafting on terrestrial debris. The strongest indication that terrestrial debris (in particular trees) may aid in transport of organisms comes from terrestrial vertebrates (reptiles). Supporting evidence comes from observations of individuals on rafts and from phylogeographic studies. Disembarkation of reptiles from rafts of terrestrial debris has been observed by Barbour (1916) and Censky et al. (1998). Several phylogeographic studies suggest over-water dispersal of terrestrial vertebrates, and in many of these cases, authors suggested rafting on terrestrial debris (Raxworthy et al. 2002, Calsbeek & Smith 2003, Carranza & Arnold 2003, Glor et al. 2005) (Figure 23). Yoder et al. (2003) suggested that Carnivora on Madagascar originated from one single dispersal event (Figure 23). They also emphasised that those groups that colonised feature ecophysiological specialisations that may have allowed relatively long trips in an unhospitable environment (e.g., a raft in the open ocean). Clearly, evidence for rafting dispersal via terrestrial debris supplied by episodic events is circumstantial. However, independent molecular studies provide increasing indication that this process may occasionally have led to successful colonisation and that it may be of major importance for the biodiversity of remote locations. Giant kelp and other substrata Due to the sporadic character of dispersal events and the fact that they may have happened far back in the past, often it is difficult or impossible to know the floating

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Figure 23 (A) Sampling sites of Anolis lizards from Caribbean islands, and (B) cladogram showing the phylogenetic relationships inferred from mtDNA data of the different Anolis species from the Caribbean islands; modified after Glor et al. (2005). (C) Proposed biogeography of carnivores from Africa and Madagascar; genetic data suggest that taxa found on Madagascar have originated from a single dispersal event from an African predecessor; modified after Yoder et al. (2003).

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substratum on which organisms have been dispersed. Some authors have used life history of present day organisms to infer potential substrata, while others have simply suggested rafting without venturing into the characteristics of rafts. Some substrata that usually travel on intermittent rafting routes (giant kelp and wood) may also sporadically be transported over distances more characteristic of episodic rafting routes. This may occur when storms or other climatic events push these substrata out of their common routes or accelerate transport velocities. During these occasions, substrata may become transported to localities that they would not normally reach. For example, giant kelp, thought to survive for several months at the sea surface, may not be capable of bridging the enormous distances of open ocean between South Africa and Australia or between New Zealand and South America. There is, however, both distributional and genetic evidence for occasional connections via floating substrata. Many coastal species are found on distant subantarctic islands and rafting on floating kelp is commonly inferred (Davenport & Stevenson 1998, Edgar & Burton 2000). A study by Waters & Roy (2004a) indicated that colonisation of Australia by the seastar Patiriella exigua resulted from a singular dispersal event from African source populations (Figure 24). This seastar also is found in the holdfasts of giant kelp, and Mortensen (1933) had suggested that dispersal of this species may occur via floating kelp. Based on phylogeographic relationships of topshell gastropods with short-lived larvae, Donald et al. (2005) suggested that repeated LDD events via rafting had occurred during the evolutionary history of these species. In the case of the species Diloma nigerrima a dispersal event between New Zealand and Chile was dated to have happened approximately 0.6 Mya, apparently too short for significant genetic divergence to take place (Figure 25). Episodic dispersal on large floating macroalgae may also play a role in the northern North Atlantic. Based on historical analyses and on the present-day distribution of important rocky-shore

Figure 24 Episodic rafting route in the West Wind Drift between Africa and Australia, possibly supported via floating giant kelp. (A) Sampling sites of different populations of Patiriella exigua; insert shows the seastar Patiriella exigua (which reproduces via benthic crawl-away larvae) from S Africa (photo courtesy of Eliecer Diaz, Rhodes University, S Africa). (B) Phylogram based on mtDNA Cytochrome Oxidase I (CO I) sequences; modified after Waters & Roy (2004a).

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Figure 25 Episodic rafting route in the West Wind Drift between New Zealand and S America, possibly supported via floating bullkelp Durvillaea antarctica. (A) Sampling sites of different gastropod species from the family Trochidae; geographic distribution of bullkelp D. antarctica indicated by light shading. (B) Phylogenetic tree based on mtDNA 16S, COI and nuclear DNA actin sequences for selected species from the S Pacific; modified after Donald et al. (2005).

organisms, Ingólfsson (1992) inferred a rafting route between northern Norway and Newfoundland and Nova Scotia on the western side of the North Atlantic, with Iceland and southern Greenland serving as intermediate stepping stones. Wares & Cunningham (2001) supported this suggestion via genetic studies. For example, they found genetic connectivity between North American and European populations of Idotea baltica (Figure 26), a species commonly found on floating algae (Ingólfsson 1995, Gutow & Franke 2003). They also revealed that the North American populations of Nucella lapillus and Littorina obtusata, with benthic crawling progeny, had originated from European populations (Wares & Cunningham 2001). In all cases rafting transport on floating algae appears to be the most likely dispersal mechanism. Ó Foighil & Jozefowicz (1999) reported phylogenetic relationships between clades of Lasaea from Florida and Bermuda on the western side of the North Atlantic and between clades from the Azores and the Iberian peninsula on the eastern side of the North Atlantic, which was confirmed in a later more extensive study (Ó Foighil et al. 2001) (Figure 27). They suggested rafting but did not mention the substrata on which these bivalves may have been transported. Regardless of whether dispersal has occurred on floating kelp, wood or other substrata, most of these studies underline the importance of episodic rafting events and subsequent periods of isolation. 368

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Figure 26 (A) The isopod Idotea baltica, which releases fully developed juveniles, on fucoid algae (photo courtesy of Veijo Jormalainen, University of Turku, Finland). (B) Map of the N Atlantic with sampling sites: M – Maine, NS – Nova Scotia, Ic – Iceland, No – Norway, Ir – Ireland, Fr – France. (C) Haplotype networks (based on mtDNA COI sequences) for populations of Idotea baltica (direct development), Nucella lapillus and Littorina obtusata (crawl-away progeny) from the N Atlantic; modified after Wares & Cunningham (2001).

Dispersal dynamics on episodic rafting routes Based on the examples presented, it appears that episodic rafting routes are most important in the tropics and in subpolar regions (Figure 17). While in the tropics these rafting routes are constituted by episodic supply of floating substrata (pumice and terrestrial debris), in subpolar regions they may represent episodic extensions of intermittent rafting routes (supported by giant kelps and wood). Interestingly, the three main substrata mentioned herein (pumice, terrestrial debris, giant kelps) appear to transport different groups or organisms. Volcanic pumice and calcareous animal skeletons are usually only colonised after starting their pelagic voyage (i.e., by marine organisms that have (short-lived) planktonic larvae). Also terrestrial debris is colonised by marine organisms while afloat, but trees or other terrestrial vegetation may additionally carry many initial terrestrial colonists such as insects, spiders or vertebrates with them to sea. In contrast, large kelps, which are colonised while growing in benthic habitats, appear to have been mainly responsible for dispersal of various marine organisms with direct development. These observations underline the importance of substratum origin and characteristics, in particular for rafting over long distances. Many authors discussed the relationship between connectivity and the possibility of population divergence. For example, Ayre & Hughes (2004) remarked on low levels of gene flow between distant local populations of corals, just sufficient to counteract genetic divergence (see above). In this context, Bryan et al. (2004) suggested pumice rafting as an important connecting process: “Speciation events and volcanicity may be linked such that the periodic development of globalism 369

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Figure 27 (A) Nest of an unidentified Lasaea species from Chile, and adult brooding juveniles. (B) Study regions of populations of Lasaea spp. in the western and eastern N Atlantic; map modified after Ó Foighil & Jozefowicz (1999). (C) The unrooted phylogram (based on mtDNA 16S sequences) showing the genetic relationships of the N Atlantic clades of Lasaea, which suggests a western and an eastern clade in the N Atlantic. Six different dispersal events were inferred between the Azores and the Iberian Peninsula (for sampling sites of eastern N Atlantic populations see detailed map); modified after Ó Foighil et al. (2001).

for some taxa (e.g., corals, gastropods, bryozoans) may correlate in time and/or space with particular igneous events”. If gene flow is insufficient, speciation processes may occur: “Species that have a capacity for sporadic dispersal may undergo dramatic range expansions followed by isolation, genetic divergence, and possible speciation” (Waters & Roy 2004a). Other authors reached similar conclusions: “…The foregoing leads to the expectation that endemism through founder speciation is most likely for organisms that rarely enter the transport medium but survive well in it” (Paulay & Meyer 2002). These authors went on to say: “Organisms that rarely enter the dispersal medium but survive well there are the most likely to undergo founder speciation. The high levels of endemicity observed in rafted, direct developing marine mollusks, and bird- and raft-dispersed terrestrial organisms support this hypothesis”. Additionally, many rafting species that survive LDD via rafting are also pre-adapted to become successful colonisers after making landfall (see Thiel & Gutow 2005b). Occasionally, rafting organisms on episodic rafting routes may even cross biogeographic borders or barriers: “The several months of transportation time provides the opportunity for biogeographic exchange, and it may be a mechanism by which biogeographic mixing in the marine realm occurs naturally” (Bryan et al. 2004). If this is followed by successful colonisation, it will lead to an enrichment of the local biota, thereby increasing local biodiversity. In general, connectivity between populations is very low on episodic rafting routes. This may, in extreme cases, lead to singular colonisation by few individuals, resulting in a founder effect. This may facilitate allopatric speciation, in particular in sexually reproducing organisms with short 370

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generation times. Furthermore, since episodic rafting routes often are supported by floating substrata of high longevity (volcanic pumice, calcareous skeletons, large trees), they may often result in LDD, transporting rafters to new habitats. Here these organisms may be confronted with established communities and conditions, exposing colonists to a selective environment different from their source regions. Thus, for several reasons dispersal via episodic rafting routes may result in rapid evolutionary changes in rafting organisms. Interrupting the sporadic pattern of these episodic rafting events may have important consequences for biodiversity.

Artificial rafting routes In this review artificial rafting routes are considered to be those sustained by floating substrata of anthropogenic origin, in particular plastics. These have gained increasing attention in recent years (Winston 1982, Barnes 2002), because supply has increased during the past century, and plastics are now present throughout the world oceans. For two main reasons, plastics do not fit the natural rafting routes discussed above: (a) they are delivered to the oceans almost anywhere, in estuaries, bays and in the open ocean, albeit with regional differences in intensity and (b) some of them are extremely long-lived and can therefore be transported over very long distances. They share some features with substrata found on frequent rafting routes (abundant supply), but they differ in other features (plastics offer no food value and are highly persistent). Similarly, some of their characteristics resemble those of substrata on episodic rafting routes (low food value and high longevity), but other characteristics are very different (plastics are supplied relatively consistently). Plastics are present on all previously described natural rafting routes, but they may gain particular importance on the intermittent and in particular on the episodic rafting routes. As outlined above, organisms on frequent rafting routes have abundant dispersal opportunities on natural floating substrata, because these are usually available in large quantities. Some of these organisms may also hitch a ride on floating plastics, but given the high connectivity between local populations already achieved via natural substrata, this may be relatively unimportant. In contrast, on intermittent and episodic rafting routes, plastics (and other anthropogenic debris) may lead to a dramatic increase in dispersal opportunities and due to their continuous supply may disrupt the sporadic character of natural dispersal events. Previous authors have suggested that episodic rafting routes, for example those sustained by volcanic pumice, may permit “periodic globalism” of some organisms (sensu Bryan et al. 2004). Chronic supply of plastics may enhance the risk of globalisation of these species and homogenisation of the species biodiversity, in particular in regions where episodic rafting events have predominated in the past, for example in the Southern Ocean (Barnes & Fraser 2003). Rafting organisms found on plastics are diverse and they include, among others, sponges, hydrozoans, bryozoans, ascidians, polychaetes, bivalves and crustaceans (Thiel & Gutow 2005b). Interestingly, corals have also been found on floating plastics or glass, including species from the genus Pocillopora, commonly reported from floating pumice (Jokiel 1984, 1989; Winston et al. 1997). This indeed indicates that plastics may serve as alternative rafting substratum for the same organisms usually transported by pumice or other sporadically supplied substrata. Floating plastics are occasionally suggested as dispersal agents connecting localities. For example, Aliani & Molcard (2003) discussed that many organisms found on floating plastics in the western Mediterranean can become widely dispersed along shorelines of this region. Winston et al. (1997) expressed similar concerns for the western South Pacific. Stevens et al. (1996) found many bryozoan species, which are usually growing on natural buoyant substrata, also on floating plastics — some rafting colonies were even sexually mature, leading the authors to infer that these species “could adapt to a pseudoplanktonic lifestyle”. Such an adaptation would then facilitate LDD. Due to their relatively recent appearance in the world oceans, no molecular study has yet identified floating plastics as potential dispersal vectors. However, given the ubiquity of plastics and other 371

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anthropogenic floating substrata and their diverse assemblage of rafters, it is considered highly likely that these may serve as connecting agents.

Rafting dispersal Marine connectivity Marine benthic invertebrates inhabit patchy environments. As described above, patches harbour local populations that may be connected by dispersal, either through larvae, rafting or other mechanisms. Connectivity among local populations of rafters will largely depend on the environmental conditions of the place they inhabit. The genetic structure of local populations is determined in part by the direction, magnitude, and frequency of dispersal among local populations. Just as it has been widely demonstrated for species with planktonic developmental stages (Palumbi 1995, Bohonak 1999), oceanographic, ecological, behavioural and historic factors may limit rafting dispersal as well. All of these factors determine the relationships between local populations and the magnitude of the effects of deterministic and random evolutionary forces (i.e., natural selection and genetic drift, respectively). Since there are several factors that, in combination, affect the dispersal potential of a species and it cannot be inferred from a single element (i.e., mode of development, Colson & Hughes 2004), estimates of gene flow have been used to understand the factors that shape connectivity among local populations. Gene flow can be indirectly estimated from population differentiation data, and represents a measure of realised dispersal potential. Gene flow estimates for a number of benthic marine invertebrates have indicated that both organisms with planktonic and direct development can achieve LDD. Larval dispersal is assumed to be the major means of dispersal for organisms with planktonic development, while rafting is considered to promote the dispersal of organisms with direct development (e.g., Johannesson 1988, Ó Foighil 1989, Davenport & Stevenson 1998). Organisms with planktonic development, too, may be dispersed through rafting, which is, however, hard to demonstrate since rafting is an explanation that often is supported indirectly by the rejection of alternative hypotheses, such as vicariance, anthropogenic and larval dispersal (e.g., Castilla & Guiñez 2000, Waters & Roy 2004a, Donald et al. 2005). Several studies stress the importance of considering the biology of a species beyond its developmental mode in order to predict its dispersal potential (e.g., Colson & Hughes 2004). While species with planktonic larvae may disperse over much shorter distances than expected from their larval lifetime, those with direct development may be transported distances far exceeding what would be expected based on their autonomous dispersal potential. Evidence is mounting that rafting can have a strong impact on the genetic structure and geographic range of distribution of some species, particularly of those with direct development. It thus may be timely not only to abolish the Rockall Paradox but also to go a step further and consider rafting as an important mechanism for the connectivity of marine communities. Use of genetic data to estimate gene flow Molecular genetic tools allow for studying the allele frequencies of populations and inferring their demographic history. There is a diversity of molecular markers, among which proteins, mitochondrial DNA (mtDNA), microsatellites and fingerprinting methods (e.g., RFLP, RAPDS) are preferred for studies on the population level (Parker et al. 1998, Sunnucks 2000, Hellberg et al. 2002, Féral et al. 2003). MtDNA has been extensively used to reveal phylogeographic patterns and population structure of a wide diversity of marine taxa (e.g., Palumbi et al. 1997, Avise 2000, Wilke & Davis 2000, Collin 2001, Breton et al. 2003, Waters & Roy 2004b). Microsatellites, proteins, and fingerprinting methods have been widely used to infer population structure often at more than one 372

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geographic scale (e.g., Edmands & Potts 1997; Ayre & Hughes 2000, 2004; Goldson et al. 2001; Colson & Hughes 2004). Many of these studies include estimates of population differentiation that also allow for estimating gene flow as the number of migrants per generation among local populations (e.g., Ayre et al. 1997, Ayre & Hughes 2000, De Matthaeis et al. 2000, Vianna et al. 2003). The genetic structure of a metapopulation depends on local dispersal dynamics influenced by both the migration rate (m) and the effective population size (N) of the metapopulation (Hellberg et al. 2002). A commonly reported measure of population differentiation is the fixation index, FST , developed by Wright (1931, 1965) that refers specifically to the differentiation among subpopulations (S) of the total population (T) and allows for the estimation of Nm (the product of effective population size and migration rate). Nm is interpreted as the number of migrants per generation, and can be calculated from FST -values by the following relationship: FST = 1/(1 + 4Nm) (Wright 1969). Generally, FST-values smaller than 0.2 (Nm = 1) represent less than one individual migrant per generation, which is considered insufficient to prevent population differentiation. Values of Nm greater than 1, corresponding to slightly higher levels of gene flow, are high enough to prevent differential fixation of alleles in different subpopulations (Wright 1969). Since many studies have reported FST values at a wide variety of spatial scales, it is used in the present analysis as a measure for comparison of genetic differentiation data from the literature. FST is a powerful tool to estimate genetic differentiation among populations. Populations at or close to equilibrium conditions will behave somewhat like the model underlying the FST coefficient and thus its value will be biologically meaningful. Caution needs to be used, though, because FST values could be misleading and in particular for populations, which commonly deviate from equilibrium assumptions underlying the mathematical model that FST is based on (see Grosberg & Cunningham 2001). Whitlock & McCauley (1999) address the general limitations of the model and its unrealistic biological assumptions that may affect the meaningfulness of the numerical value. Based on their analysis, they suggest that “comparisons of large groups of species are likely to be more informative, as many of the differences may average out” (see also Neigel 1997, 2002). In the present review, such an analysis is undertaken, and genetic structure data are compiled and analysed for a large group of marine invertebrates. FST approaches have revealed patterns of genetic structure over a wide range of biological scenarios and have indicated that the genetic structure of populations is shaped by several factors, including gene flow barriers that are thought to be due to environmental factors (see below). Data should be carefully interpreted; in some cases genetic differentiation of populations may be reflecting historic rather than ongoing events. For example, gastropod species of the genus Nucella with similar dispersal potentials (they lay egg capsules from which juveniles emerge) display extremely different patterns of population structure across the same geographic range (Marko 2004). Usually these differences have been attributed to dispersal potential, but in this case, the species have similar dispersal potentials based on their developmental mode. The results of that study address the importance of ecological and historical differences for the genetic structure of populations. FST cannot detect gene flow asymmetry as it only shows a measure of total differentiation among populations without considering independently the contribution of each of the compared populations to the differentiation among them. Measures of asymmetric gene flow are particularly desirable in the context of rafting, and can be predicted by some alternative means, although these are scarce in the literature. An example is given by Wares et al. (2001) who used a cladistic analysis to detect asymmetrical migrations. They studied genetic differentiation of two barnacle species and a sea urchin across Point Conception in California, which had been suggested as a strong barrier to gene flow. The cladistic approach allowed them to determine that there was an excess of southward migration events across Point Conception. In the context of rafting it is desirable to have estimates of magnitude and direction of dispersal among local populations of potential rafters to better understand the dynamics of rafting routes. In cases of unique rafting events that lead to allopatric speciation (on episodic routes), the direction of the dispersal route can be detected with phylogenetic 373

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analyses. Intermittent and frequent rafting routes, however, prevent speciation by maintaining sufficient connectivity among local populations. In these cases, the genetic structure of populations will depend on the magnitude and direction of migration, even though asymmetrical gene flow is not often detected, total gene flow estimates (Nm) can be inferred (from FST values) and are likely to reflect the summed contributions of populations or groups of populations to the total exchange among them. There exists a variety of other measures of population differentiation that alleviate many of the problems associated with FST, but most are scarcely reported in marine population genetic studies and thus are not useful for comparison of a large number of studies. The numerous reports of FST-like values allow estimation of realised dispersal of many marine taxa (Neigel 1997, Bohonak 1999) and will be used herein to make broad comparisons of the dispersal potential of benthic marine invertebrate taxa. Genetic homogeneity vs. genetic structure of populations Even though marine environments seem to lack apparent barriers to gene flow, populations only sometimes show panmixia and genetic differentiation exists even when wide dispersal is predicted based on larval developmental mode. Marine populations usually show reduced heterozygosity (e.g., Ayre & Hughes 2000), explained largely by the restricted dispersal of marine organisms and consequent effects of inbreeding and local population differentiation, which can generate a Wahlund effect (i.e., decreased heterozygosities resulting from the sampling of subdivided populations) (e.g., Johnson & Black 1984a). Planktonically developing taxa intrinsically provide good models to study the potentially restricting effects of the environment on gene flow. Several factors such as oceanographic conditions, physical barriers, life-history features, historic demography and ecological or behavioural barriers can hinder the realised dispersal of marine taxa (Hedgecock 1986, Palumbi 1994). The same barriers that have been described for species with planktonic dispersal should apply to dispersal through rafting, too. Many studies have detected limited gene flow in species that presumably have a high potential for dispersal. There are many factors that can act as gene flow barriers and that promote geographic differentiation. Gene flow barriers can be inferred from genetic structure and population differentiation data. For example, Sköld et al. (2003) found that genetic differentiation of populations of the widely dispersing seastar Coscinasterias muricata in the New Zealand fjords is not correlated with geographic distance. They suggested that recent colonisation and isolation from open coasts explain the apparent island model of the population. Perrin et al. (2004) also studied population differentiation of this species along the New Zealand fjords and found that at a macrogeographical scale (>1000 km) there was restricted gene flow between the North and South Island. At a mesogeographical scale (tens to hundreds of km) there was significant population differentiation among fjords and the open coast. The pattern among fjords suggests that populations from the north and the south meet in what appears to be a secondary contact zone. For this species, distance alone does not explain population differentiation and it is likely that hydrography prevents mixing of propagules and contributes to isolation of local populations. Local populations seem to have expanded recently and subsequently differentiated as a consequence of isolation. Perrin et al. (2004) suggest that once the larvae of C. muricata “are transported out of the fjord, the likelihood of entering another fjord is less than being transported further along the open coast. For this species, the fjords might act as barriers to dispersal of differing strength, facilitating genetic drift within fjord populations.” Along the New Zealand coast, Waters & Roy (2004b) found that upwelling in the central regions blocks gene flow and leads to genetic differentiation between the populations of the seastar Patiriella regularis from the north and south that are subject to different oceanographic conditions. Just as upwelling can transport propagules away from coastal systems, it may bring propagules toward the coast when it reverses its direction (Palumbi 2003). It is likely that if an 374

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upwelling zone poses a barrier to gene flow in species with planktonic development, it will also affect the connectivity of populations of rafters. Habitat structure may highly influence population structure, sometimes because different habitats may differ in the rafting opportunities they offer (see above). Johannesson & Tatarenkov (1997) found that the population structure of the brooding gastropod Littorina saxatilis on islands of the Swedish coast was highly related to habitat structure. Similarly, Johannesson et al. (2004) reported that genetic structure among L. saxatilis on high rocky shores was different from the ones on low rocky shores. Populations on high rocky shores appear to be more isolated which, as stated by the authors, “might be true if the main mechanism of dispersal among islands is by rafting”. Some studies show the prevailing pattern, namely that populations of organisms with extensive planktonic larval stages are not genetically subdivided. For example, the marine bryozoan Membranipora membranacea does not show genetic differentiation among populations across the Atlantic Ocean, even though there is morphological variation caused by phenotypic plasticity (Schwaninger 1999). Surprisingly, this species seems to maintain gene flow over long geographic stretches, which could be due to rafting (it has been reported on floating substrata, see Aliani & Molcard 2003) or other mechanisms (e.g., human transport). Conversely, other studies have shown that species with direct development tend to be highly structured due to restricted gene flow (e.g., Hellberg 1994, Ayre et al. 1997, McFadden 1997). This seems to be the case in the gorgonian coral Pseudopterogorgia elisabethae, which has restricted dispersal potential (larvae live less than two days) and shows high genetic differentiation among populations following an IBD pattern (Gutiérrez-Rodríguez & Lasker 2004). Contrary to expectations based on developmental mode alone, there are examples of directly developing species that show that LDD has taken place or that there is little differentiation among populations. For example, the direct developers Littorina sitkana and Nucella lapillus display high levels of gene flow over relatively wide geographic scales (>1500 km) (Kyle & Boulding 2000, Colson & Hughes 2004) (Figure 16). Based on the above, it becomes evident that connectivity cannot be predicted solely on the basis of mode of development (see also Ó Foighil et al. 1999, Colson & Hughes 2004).

Rafting-mediated gene flow In the past, dispersal rates have been frequently inferred based on presence/absence and duration of a planktonic dispersal stage. However, there are many examples of organisms with planktonic development that, based on population differentiation, have restricted dispersal among local populations (e.g., Barber et al. 2000, McCartney et al. 2000). On the other end of the scale, species that lack a planktonic dispersal stage may disperse long distances by alternative means such as rafting. Comparisons of gene flow estimates from a wide variety of benthic marine taxa clearly show that populations of organisms with contrasting modes of dispersal can achieve comparable levels of gene flow and that rafting is a significant means of dispersal at more than one spatial scale, particularly for species with direct development (see below). Rafting has been inferred for 33 out of 124 marine invertebrate species for which genetic differentiation data are available (Table 1). In many of the studies, rafting was inferred because realised gene flow strongly exceeded the expectations based on life history characteristics (i.e., absence of a planktonic larval stage), or because of the absence of IBD in brooders suggested the existence of LDD. For 113 of the 124 reviewed species data were reported that allowed an examination of realised gene flow over variable spatial scales (from metres to global distribution) (Table 1). Only reports that include FST-like values have been incorporated in this analysis. From the FST-like values given, gene flow (Nm; number of migrants per generation) was estimated according to the equation of Wright (1969) (Table 1). Whenever possible, genetic differentiation data for more than one geographic scale were recorded for each species (see Table 1). Values of 375

376

P

P

D

P

A. millepora

A. nasuta

A. palifera

A. palmata

D

Anthozoa Acropora cuneata

P

P

Hydrozoa Obelia geniculata

A. hyacinthus

D

Haliclona sp.

P

L

Porifera Crambe crambe

A. cytherea

Dev.

Species

E Australia, GBR E Australia, GBR

Allozymes Allozymes

Microsatellites Caribbean and Bahamas

NE Australia, GBR E Australia, GBR

E Australia, GBR

Allozymes

Microsatellites and ncDNA Allozymes

E Australia, GBR and Lord Howe Island

N Atlantic

Mediterranean, Madeira and Canary Islands SW Australia

Allozymes

mtDNA

Microsatellites ncDNA mtDNA Allozymes

Genetic system

Geographic location

840

1800

2400 1700 1200 8 1200 8 1200 8 1200 8 500 35 1200 8 >3000

5000

3000 3000 3000 400

Spatial scale (km)

θ = 0.29 θ = 0.08 θ = 0.05 θ = 0.15 θ = 0.03 θ = 0.08 θ = 0.05 θ = 0.07 θ = 0.01 θ = 0.1 FST = 0.034 FST = 0.025 θ = 0.02 θ = 0.09 θ = 0.036 RST = 0.153 θ = 0.04 RST = 0.221 θ = 0.032 RST = 0.150

FST = 0.26

θ = 0.18 % var = 9.78 FST = 0.565 θ = 0.121

Genetic structure

7.56

6

0.61 2.87 4.75 1.42 8.08 2.89 4.75 3.32 24.75 2.25 7.1 9.75 12.25 2.53 6.69

0.71

0.19 1.82

1.14

Nm

No No No data

Yes No No No No No No No No No No data

No data

Yes Yes No No data

IBD

Table 1 Genetic structure of populations of several marine invertebrate taxa reported in the literature

Ayre & Hughes 2000 Ayre & Hughes 2000 Baums et al. 2005

No No

No

No

No

No

Ayre & Hughes 2004 Ayre & Hughes 2004 Ayre & Hughes 2000 Ayre & Hughes 2000 Ayre & Hughes 2000 Ayre & Hughes 2000 Ayre & Hughes 2000 Ayre & Hughes 2000 Ayre & Hughes 2000 Ayre & Hughes 2000 Mackenzie et al. 2004

Govindarajan et al. 2005

Duran et al. 2004a Duran et al. 2004b Duran et al. 2004c Whalan et al. 2005

Reference

No

Yes, on seaweeds

No

No

Rafting inferred

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Allozymes Allozymes

P

P

D

Anthopleura elegantissima Anthothoe albocincta Balanophyllia elegans

377

D

D

P

P

E. prolifera

E. ritteri

Oulactis muscosa

Paracyathus stearnsii

SE Australia

Allozymes California

NE Pacific

Allozymes

Allozymes

NE Pacific

NE Pacific

NE Australia, GBR

Brazil

California

SE Australia

NE Pacific

Bermuda and Brazil Brazil SE Australia NE Pacific

E Australia, GBR and Lord Howe Island

Allozymes

Allozymes

Allozymes

D

D

Allozymes

Allozymes Allozymes

P

Epiactis lisbethae

Bunodosoma caissarum Clavularia koellikeri

Allozymes

P D

A. tenebrosa Alcyonium rudyi

Allozymes

D

Actinia bermudensis

Allozymes

P

A. valida

735 0.024 1000 100

1800

1800

1000 30 4 1800

1150

3000 1000 100

930

2500 1700 1200 8 4000 2000 1150 1050 1100 600 50 1800

0.64 0.87 1.03 5.7 2.53 1.62 1.07 0.44 0.53 1.31

θ = 0.28 θ = 0.22 θ = 0.195 FST = 0.042 0.09 0.134 0.189 0.36

θ θ θ θ θ = 0.32 θ = 0.16 FST = 0.0295 FST = 0.0045 θ=0 θ = 0.004

8.23 55.31 very large 63.25

0.61

θ = 0.29

= = = =

0.94 6.33 12.25 0.64 0.33 0.94 2.33 0.42 0.58 0.49 0.61 1.54

θ = 0.21 θ = 0.038 θ = 0.02 θ = 0.28 FST = 0.434 FST = 0.21 FST = 0.262 FST = 0.375 θ = 0.3 θ = 0.34 θ = 0.29 θ = 0.14

No data No data No

No Info

No Info

No Info

No

Yes

Yes

No

No

Yes, on eelgrass or algae Yes, on eelgrass or algae Yes, on eelgrass or algae No

No

Yes, on macroalgae (Bushing 1994) No

Yes, on eelgrass or algae No

No No No

Yes No No

No data

No

No

Yes No No No Yes

Hellberg 1996

Hunt & Ayre 1989

Edmands & Potts 1997

Edmands & Potts 1997

Edmands & Potts 1997

Bastidas et al. 2002

Russo et al. 1994

Billingham & Ayre 1996 Hellberg 1994 Hellberg 1996

Edmands & Potts 1997

Ayre & Hughes 2004 Ayre & Hughes 2004 Ayre & Hughes 2000 Ayre & Hughes 2000 Vianna et al. 2003 Vianna et al. 2003 Russo et al. 1994 Ayre et al. 1991 McFadden 1997

7044_C007.fm Page 377 Tuesday, April 25, 2006 1:08 PM

RAFTING AND MARINE BIODIVERSITY

378

D

P

P

Polychaeta Hediste diversicolor

Neanthes virens

Pectinaria koreni

D

Styllophora pistillata

D

P

E Australia, GBR and Lord Howe Island

Allozymes

P s.l.

Pseudopterogorgia elisabethae Seriatopora hystrix

Sinularia flexibilis

Bahamas

Microsatellites

P

Microsatellites

mtDNA

mtDNA Allozymes

Allozymes

Allozymes

Microsatellites

W Pacific, NE and NW Atlantic, N Sea British coasts and English Channel

N Atlantic and Mediterranean

E Australia, GBR and Lord Howe Island

GBR NE Australia, GBR

SW Australia Indo-W Pacific

E Australia, GBR

P. meandrina

Allozymes

D

Pocillopora damicornis

Genetic system

Dev.

Species

Geographic location

200

5500 2500 175 >30,000

2400 1700 1200 8 90 1300 30 4 2400 1700 1200 8

2400 1200 8 400 2000 7.5 450

Spatial scale (km)

θ = 0.19 θ = 0.23 θ = 0.15 θ = 0.28 FST = 0.43 θ = 0.0065 θ = 0.026 θ = 0.041 θ = 0.15 θ = 0.026 θ = 0.09 θ = 0.18

FST = 0.04

6

0.47 2.33

1.067 0.84 1.42 0.64 0.33 38.21 9.37 5.85 1.42 9.37 2.53 1.14

θ = 0.15 θ = 0.01 θ = 0.04 FST = 0.165 θ = 0.056 θ = 0.019 θ = 0.48

% var = 45.3 θ = 0.347 θ = 0.097 % var = 0

Nm 1.42 24.75 (31) 6 1.27 4.21 12.91 0.27

Genetic structure

No

No data Yes No No data

Yes No No No

Yes No No No No data No

Yes

Yes No No No Yes

IBD

No

No

No

No

No

No

No

No

Yes, on pumice (Jokiel & Cox 2003)

Rafting inferred

Table 1 (continued) Genetic structure of populations of several marine invertebrate taxa reported in the literature

Reference

& & & &

Hughes Hughes Hughes Hughes

2004 2004 2000 2000

Jolly et al. 2003a

Breton et al. 2003 Virgilio & Abbiati 2004 Breton et al. 2003

Ayre Ayre Ayre Ayre

Gutiérrez-Rodríguez & Lasker 2004 Ayre & Hughes 2004 Ayre & Hughes 2004 Ayre & Hughes 2000 Ayre & Hughes 2000 Ayre & Dufty 1994 Bastidas et al. 2001

Ayre & Hughes 2004 Ayre & Hughes 2000 Ayre & Hughes 2000 Stoddart 1984 Magalon et al. 2005

7044_C007.fm Page 378 Tuesday, April 25, 2006 1:08 PM

MARTIN THIEL & PILAR A. HAYE

379 RAPD RAPD Allozymes Allozymes

D

D

Idotea chelipes

Allozymes Allozymes

D

D P

Synalpheus brooksi S. pectiniger

mtDNA

Peracarida Corophium volutator Gammarus locusta

P

ncDNA

P

Scylla serrata

mtDNA Microsatellites

P P

mtDNA

mtDNA

P

Hoplocarida Haptosquilla pulchella

mtDNA mtDNA and ncDNA mtDNA

P

P

Chthamalus fissus

Eucarida Callinectes bellicosus Euphausia superba Lithopenaeus setiferus Penaeus monodon

P

Cirripedia Balanus glandula

SE British coastal lagoons

Portugal

Gulf of Maine

E Indian Ocean and Red Sea Caribbean Caribbean

Circumantarctic W Atlantic and Gulf of Mexico W Indian Ocean and W Pacific

E Pacific

Indo-W Pacific

California

California

100

500

160

4800 4800

2000 >7500 >7500 8000

>7000 4700

600

5000

800

1600 1500

0.075 0.505 0.398 0.04

FST = 0.074 FST = 0.057 FST = 0.164

ΦST = 0.205

θ = 0.54 θ = 0.14

= = = =

1.27 4.14 1.27

0.97

0.21 1.54

3.08 0.25 0.38 6

11.65 12.25

ΦST = 0.021 FST = 0.02 FST FST FST FST

very large

ΦST = 0

0.037

5.31 (*1.9)

θ = 0.045 ΦST = 0.87

5.31 (*7.35) 0.41

θ = 0.045 ΦST = 0.38

No data No data No data

No

No data No data

No

No data Yes, weak No data

No

No

No data

No data

Yes, on macroalgae Yes, on macroalage

No

No No

No

No

No No

No

No

No

No

Costa et al. 2004 Coelho et al. 2002 Jolly et al. 2003b

Wilson et al. 1997

Duffy 1993 Duffy 1993

Fratini & Vannini 2002

Duda & Palumbi 1999

Zane et al. 1998 Ball & Chapman 2003

Pfeiler et al. 2005

Barber et al. 2002

Wares et al. 2001

Wares et al. 2001 Sotka et al. 2004

7044_C007.fm Page 379 Tuesday, April 25, 2006 1:08 PM

RAFTING AND MARINE BIODIVERSITY

380 Allozymes

D

D

D

D

D

J. ischiosetosa

J. nordmanni

J. praehirsuta

Orchestia montagui O. stephenseni

Platorchestia platensis

Paracorophium excavatum P. lucasi

Allozymes

D

J. forsmani

Allozymes

Allozymes

D

D

Allozymes

D

Allozymes

Allozymes

Allozymes

Allozymes

Allozymes

D

Jaera albifrons

Genetic system

Dev.

Species

Mediterranean

New Zealand

New Zealand

>3000

1600

1600

>3000

0.13 3.27

FST = 0.66 θ = 0.071

0.11

0.30

θ = 0.452

Mediterranean

Mediterranean

Anglesey, UK

Anglesey, UK

Anglesey, UK

FST = 0.7

4.21 5.07 27.53 3.99 4.85 22.48 3 4.75 8.67 0.96 1.19 7.33 1.01

GPT = 0.056 GPT = 0.047 GPT = 0.009 GPT = 0.059 GPT = 0.049 GPT = 0.011 GPT = 0.077 GPT = 0.050 GPT = 0.028 GPT = 0.207 GPT = 0.174 GPT = 0.033 θ = 0.198

200 100 0.06 200 100 0.06 200 100 0.06 200 100 0.06 >3000

2.53

GPT = 0.09

0.06 Anglesey, UK

7.56

GPT = 0.032

100

Anglesey, UK

Yes, but weak No

Yes

No

Yes

No data

No data

No data

No data

Yes, on macroalgae

No

Yes, on macroalgae Yes, on macroalgae No

No

No

No

No

No

No data

2.76

FST = 0.083

100

No

No data

1.82

GPT = 0.121

South Wales

Rafting inferred

IBD

Nm

Genetic structure

200

Spatial scale (km)

Anglesey, UK

Geographic location

Table 1 (continued) Genetic structure of populations of several marine invertebrate taxa reported in the literature

De Matthaeis et al. 2000

Stevens & Hogg 2004

De Matthaeis et al. 2000 De Matthaeis et al. 2000 Stevens & Hogg 2004

Carvalho & Piertney 1997

Carvalho & Piertney 1997

Carvalho & Piertney 1997

Carvalho & Piertney 1997 Piertney & Carvalho 1994 Carvalho & Piertney 1997 Carvalho & Piertney 1997 Carvalho & Piertney 1997

Reference

7044_C007.fm Page 380 Tuesday, April 25, 2006 1:08 PM

MARTIN THIEL & PILAR A. HAYE

381

mtDNA mtDNA mtDNA mtDNA mtDNA Allozymes mtDNA

D

D

L

P P P

P

D

D

H. ventrosa

Littoraria angulifera Allozymes

mtDNA

Allozymes

CJ

Cominella lineolata Crepidula atrasolea C. convexa Northern species C. convexa Southern species C. depressa C. fornicata Echinolittorina lineolata** Hydrobia ulvae

Allozymes

P

Allozymes Allozymes

CJ

Prosobranchia Bedeva hanleyi

Allozymes

mtDNA

D

D

Talitrus saltator

Cerithium lividulum C. vulgatum

D

Sphaeroma terebrans

NW European coasts NW European coasts and Mediterranean Brazil

NW Atlantic NW Atlantic Brazil

NW Atlantic

NW Atlantic

SE Australian coast NW Atlantic

Mediterranean

SE Australian coast Mediterranean

Mediterranean

E Africa and Florida USA

4000

6000

6000

1300 2600 4000

4500

1300

1300

162

1750

1750

180

>3000

30,000 500

0.36

1.1

FST = 0.185

0.75

4.38

0.23

1.33

0.18

FST = 0.41

FST = 0.25

APV= -7,4 APV= 22.1 FST = 0.054

APV= 87.2

APV= 76.1

APV= 54.3

FST = 0.52

FST = 0.158

FST = 0.582

1.54

0.05

θ = 0.843

FST = 0.14

0.04 0.18

FST = 0.85 FST = 0.58

No

Yes

No

No No Yes

Yes

Yes

Yes

May be

No data

No data

May be

Yes

No

Yes, on mangrove trees (David Reid, pers. comm.)

Yes

Yes

No No No

Yes, on seagrass

No

Yes

No

No

Yes

Yes, on mangrove woods Yes, on macroalgae

Andrade et al. 2003

Wilke & Davis 2000

Wilke & Davis 2000

Collin 2001 Collin 2001 Andrade et al. 2003

Collin 2001

Collin 2001

Collin 2001

Boisselier-Dubayle & Gofas 1999 Boisselier-Dubayle & Gofas 1999 Hoskin 1997

Hoskin 1997

De Matthaeis et al. 2000

Baratti et al. 2005

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RAFTING AND MARINE BIODIVERSITY

382

D

Nucella lamellosa mtDNA haplot. mtDNA seq.

mtDNA

P

P D

L. scutulata L. sitkana

NE Pacific SE Australian coast S Australia, Tasmania and New Zealand NW Pacific

Koster archipelago W Swedish coast

Swedish coast NE Pacific W Swedish coast

mtDNA Allozymes

Allozymes mtDNA Allozymes

NW Australia

D P

P P D

L. littorea L. plena L. saxatilis

Allozymes

Brazil

L. subrotundata Morula marginalba Nerita atramentosa

P

Littorina cingulata

Allozymes

Genetic system

W Swedish coast NE Pacific NE Pacific

P

L. flava

RAPD mtDNA mtDNA

Dev.

Species

Geographic location

5000

2000

3600 162

150 745 3600

300 75

1500 1120 160 300 245 300

4000

Spatial scale (km)

FST = 0.031 FST = 0.021 FST = 0.013 GPT = 0.021 ΦST = 0.065 GPT = 0.078

1.83 14.46

ΦST = 0.12 FST = 0.017

% var = 0.06 % var = 0.11

% var = 0.84

Very large Very large

% var = 8.6 ΦST = 0 ΦST = 0

2.38 2.88

7.81 11.66 18.98 11.66 3.6 2.96

FST = 0.028

GPT = 0.095 GST = 0.008

Nm 8.68

Genetic structure

Yes

No

Yes May be

Yes No No

No data Yes

No No Yes No No Yes

Yes

IBD

No

No

No Yes, on intertidal rockweeds (Fucus distichus) No Yes

No No Yes (Johannesson et al. 2004)

Yes, on mangrove trunks (David Reid, pers. comm.) No

Rafting inferred

Table 1 (continued) Genetic structure of populations of several marine invertebrate taxa reported in the literature

Reference

Marko 2004

Waters et al. 2005

Kyle & Boulding 2000 Hoskin 1997

Janson 1987b Johannesson & Tatarenkov 1997 Johannesson et al. 2004 Kyle & Boulding 2000 Kyle & Boulding 2000

Janson 1987a Kyle & Boulding 2000 Janson 1987a

Johnson & Black 1998

Andrade et al. 2003

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MARTIN THIEL & PILAR A. HAYE

383 mtDNA Allozymes

P

D

P

Cephalopoda Pareledone turqueti

Asteroidea Acanthaster planci Allozymes

Allozymes

mtDNA

P

Allozymes

Allozymes

Spisula s. solidissima Tridacna maxima

P

Goniodoris nodosa

Allozymes

P

L

Opisthobranchia Adalaria proxima

Macoma balthica

P

Siphonaria jeanae

mtDNA haplot. mtDNA seq. Allozymes

P

D

N. ostrina

Microsatellites

Bivalvia Donax deltoides

D

N. lapillus

E Pacific and Indian Oceans, GBR

South Georgia

Indo-W Pacific

N Europe and Alaska NW Atlantic

SE Australia

British Isles

British Isles

W Australia

NW Pacific

British coasts

700 10,000

0.15

>5000 2600 1000

1000

Spatial scale (km)

= = = =

0.62 0.46 0.02 0 θ = 0.04 θ = 0.1 θ = 0.06

θ θ θ θ

θ = 0.0008 % div = 0.9 % div = 1.8 % div = 3.2 θ = 0.462 FST = 0.072

6 2.25 3.92

0.15 0.29 12.25 very large

0.29 3.22

312.25

3.85 9.75 0.96 (1.9) 0.87 (1.7) 124.75

1.4

ΦST = 0.152 FST = 0.061 FST = 0.025 θ = 0.206 ΦST = 0.224 θ = 0.002

0.38

Nm

FST = 0.395

Genetic structure

No Yes No

No

No data

No Yes

No No data

No

Yes

Yes

Yes

IBD

No

No

No

No

No

No Yes, on macroalgae or wood

No

(Yes), personal comments by R. Emson Yes (Waters & Roy 2003)

Rafting inferred

Table 1 (continued) Genetic structure of populations of several marine invertebrate taxa reported in the literature

Lessios et al. 2001

Lessios et al. 2001

Lessios et al. 2001

Lessios et al. 2001

Hunt 1993 Waters & Roy 2004b

Williams & Benzie 1998 Williams & Benzie 1996 Hunt 1993 Waters & Roy 2004a

Sköld et al. 2003

Perrin et al. 2004

Baus et al. 2005

Reference

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MARTIN THIEL & PILAR A. HAYE

Allozymes and mtDNA

P

385

D

Ectoprocta (Bryozoa) Alcyonidium L gelatinosum

Ophiuroidea Amphipholis squamata

British Isles

W Mediterranean

RAPD

RAPD

New Zealand

NE Pacific NE Pacific

California

Caribbean and Brazil Indo-W Pacific Indo-W Pacific E Pacific Caribbean Australia and Tasmania E Australia SW Europe

N Pacific Ocean Islands

RFLP and mtDNA

mtDNA mtDNA

RFLP mtDNA

P P

P D

mtDNA mtDNA mtDNA mtDNA RFLP

P P P P P s.l.

Holothuroidea Cucumaria miniata C. pseudocurata

mtDNA

P

Echinometra lucunter E. mathaei E. oblonga E. vanbrunti E. viridis Heliocidaris erythrogramma H. tuberculata Paracentrotus lividus Strongylocentrotus purpuratus

Allozymes and mtDNA

P

Echinothrix diadema

800

0.003

1600

2350 2300

870

>10,000 >10,000 4700 2600 3400 1500 3400 5000

>5000 >5000 2000 10,000

= = = = 0.064 0.01 0.022 0.261

3

1.42

FST = 0.15

FST = 0.077

0.31

4.75 (10) 0.01 (0.017)

8.08

0.39 0.57 4.14 0.44 0.15 0.49 1.83 24.75

3.66 24.75 11 0.71

Φ = 0.45

ΦST = 0.05 ΦST = 0.97

FST = 0.03

FST = 0.389 FST = 0.306 FST = 0.057 FST = 0.361 GST = 0.62 GST = 0.34 GST = 0.12 FST = 0.01

FST FST FST FST

No data

No

Yes, but low

No data No data

No data

No data No

Yes Yes No data No data No data

No data

No data

Yes, on algae

Yes, on macroalgae or debris (Sponer & Roy 2002)

No Yes, on surf grass Phyllospadix scouleri

Yes, on algae (Hobday 2000a)

No No

No No No No No

No

No

Porter et al. 2002

Féral et al. 2001

Sponer & Roy 2002

Arndt & Smith 1998 Arndt & Smith 1998

Edmands et al. 1996

McMillan et al. 1992 Duran et al. 2004d

Palumbi et al. 1997 Palumbi et al. 1997 McCartney et al. 2000 McCartney et al. 2000 McMillan et al. 1992

McCartney et al. 2000

Lessios et al. 1998

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RAFTING AND MARINE BIODIVERSITY

386 Allozymes Allozymes Allozymes

D

P

D

Allozymes

SE Australia

SE Australia

SE Australia

NE Pacific, NE and NW Atlantic

North Wales

British Isles North Wales

140

215

190

14,000 4600 2200

10

1500 10

Spatial scale (km)

FST = 0.210

FST = 0.002

FST = 0.202

θ = 0.726 θ = 0.019 θ = 0.014

% var = 0

FST = 0.105 % var = 5.29

Genetic structure

0.94

124.75

0.99

0.09 12.91 17.61

2.13

Nm

Yes

No

Yes

No data

No

No data Yes

IBD

No

No

No

Yes, on algae (Vallentin 1895, Todd et al. 1998) Yes, on plastic (Aliani & Molcard 2003)

No No

Rafting inferred

Ayre et al. 1997

Ayre et al. 1997

Ayre et al. 1997

Schwaninger 1999

Goldson et al. 2001

Porter et al. 2002 Goldson et al. 2001

Reference

Dev. = mode of development; P = planktonic development; D = direct development; L = short-lived lecitotrophic larvae; CL = crawling larvae; CJ = crawling juveniles; s.l. = short lived; mtDNA = mitochondrial DNA; ncDNA = nuclear DNA; % var = percentage of molecular variance; % div = percentage sequence divergence; APV = among population variance; approximately equal to FST (Excoffier et al. 1992); AGD= average genetic diversity; GPT = coefficient of gene differentiation between populations; * = CME or cladistic migration events; **species reported by author under a different name.

Notes: Most studies provided an FST-like measure of population genetic differentiation. For each species information is included about its mode of development, molecular marker (genetic system) used to infer population structure, geographic location of the studies, spatial scales for which population genetic differentiation data are available (most were calculated from maps or coordinates provided in the literature), estimates of genetic differentiation (genetic structure) among populations (original parameter given by authors is presented), presence or absence of an isolation by distance pattern (IBD), whether rafting has been inferred for the taxon and references of the genetic studies from which population differentiation data was obtained. Nm was calculated using the equation of Wright (1969) (see text). Values of Nm provided by the authors that differ from those calculated by us are given in parentheses.

Tunicata Botrylloides magnicoecum Pyura gibbosa gibbosa Stolonica australis

P

RAPD

P

Membranipora membranacea

RAPD RAPD

P L

A. mytili Celleporella hyalina Electra pilosa

Genetic system

Dev.

Species

Geographic location

Table 1 (continued) Genetic structure of populations of several marine invertebrate taxa reported in the literature

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RAFTING AND MARINE BIODIVERSITY

Nm and geographic scale for which differentiation values where available were classified by mode of development of the studied species. The direct development categories included all organisms that brood their progeny up to a juvenile or crawl-away stage or that have very short-lived larvae (5,000

6

10

16

3

21

21

35

4

4

12

26

12

Connectivity (Nm)

High Nm (>10)

Medium Nm (1-10)

Low Nm (5000 km) can be further explored in Figure 29 where data are presented as the number of species of each of the four broad categories that achieve high (>10), intermediate (1–10) and low (3000 km) and whose haplotypes are more divergent than the ones from closer islands. Even though episodic raftingmediated gene flow is inferred for this species, local levels of connectivity are low enough to allow genetic differentiation (Colgan et al. 2005). Indeed, “the population structure of P. exigua indicates that effective recent migration between New South Wales, Tasmania and South Australia has been so low that complete lineage sorting of haplotypes to regions has occurred” (Colgan et al. 2005). There are also a few species with planktonic development that are inferred to raft, and where rafting may contribute to connectivity at this scale. For example, the actiniarian Anthopleura elegantissima, distributed from British Columbia to Southern California, is suggested to raft on eelgrass or algae and 1.54 migrants per generation are inferred from genetic differentiation data (Edmands & Potts 1997). The bryozoan Membranipora membranacea, frequently found growing on positively buoyant kelp and plastics, exchanges more than 15 individuals per generation at a scale >3000 km. The snail Littoraria flava may disperse by rafting at this geographic scale as it lives on mangrove trunks (as well as rocks) (David Reid, personal communication) and high connectivity among populations located 4000 km apart corresponds to 8.68 migrants per generation (Andrade et al. 2003). Rafting may also contribute to the connectivity of the populations of the seastar Coscinasterias muricata at this geographic scale (Waters & Roy 2003). Distances involved (1000–5000 km) may be extensive requiring long voyages (possibly exceeding the lifetime of planktonic larvae of many species), and rafting may permit some connectivity among their populations at these geographic distances. Particularly interesting is the case of the widely distributed hydrozoan Obelia geniculata. This species has a relatively short-lived lecitotrophic planula larvae and the asexually produced medusa lives for approximately 1 month (Stepanjants et al. 1993, cited in Slobodov & Marfenin 2004). At least for the White Sea, these medusae are expected to disperse only for about 3–4 km, but the dispersal distance will depend on the speed and direction of the currents (Sergei Slobodov, personal

393

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communication). The hydroids grow on various substrata, including macroalgae, offering the possibility for rafting. In fact, O. geniculata has been inferred as a rafter in many regions of the world (see references in Thiel & Gutow 2005b). Within the North Atlantic and based on genetic data, Govindarajan et al. (2005) proposed as the most likely scenario that populations from Canada and Iceland had been sheltered in northern glacial refugia, and subsequently expanded southward. In general they found high genetic differentiation among the four North Atlantic populations studied (Massachusetts, New Brunswick, Iceland and France), with the exception of the New Brunswick and Iceland populations, which also share many unique haplotypes (Figure 30). This further supports the suggestion of a rafting route connecting the North American and Icelandic populations (see also Ingólfsson 1992, Wares & Cunningham 2001). The Massachusetts population, on the other hand, only has haplotypes shared with New Brunswick, suggesting recent southern expansion of the New Brunswick population (Govindarajan et al. 2005), possibly also achieved through rafting. In summary, rafting has been invoked as an important means of dispersal for many species at the geographic scale of 1000–5000 km, showing an impact on the realised dispersal among populations of directly developing species (Figure 28 and Figure 29). Most of the examples given above correspond well with the predictions of intermittent rafting routes, bearing in mind that some of these routes may be stronger or more permanent in time than others and that this leads to varying levels of connectivity among populations at this geographic scale. These rafting routes are crucial for direct-developing species whose metapopulation structure is controlled by migration at this macrogeographic scale. Rafting-mediated connectivity at the geographic scale >5000 km At a wider geographic range (>5000 km), rafting does not seem to be a prevalent mechanism of dispersal, and when inferred it only contributes with low levels of gene flow, presumably through episodic rafting routes that may sometimes connect distant populations while others found new populations, thus expanding the geographic range of distribution or contributing to allopatric speciation. The small but existent migration among populations of the isopod Sphaeroma terebrans across oceans might be achieved through rafting, and as stated by the authors, “In spite of the low vagility of S. terebrans, mechanisms of passive dispersal, probably through floating mangrove woods, could be responsible for the worldwide distribution of the taxon, which is until now considered cosmopolitan” (Baratti et al. 2005). They conclude that current patterns also affect “mangrove fragments with animals on board” resulting in genetic differentiation patterns, and that their reproductive strategy “is not sufficient to produce a high level of reproductive isolation between S. terebrans populations since passive dispersal through floating mangrove wood transported by currents could maintain a certain degree of gene flow between populations” (Baratti et al. 2005) (Figure 12). However, it cannot be excluded that this wood-boring isopod may not also be transported via anthropogenic vectors (e.g., on wooden ships). Rafting has been suggested as a means of dispersal at a scale over 6000 km for two gastropod species of the genus Hydrobia from the European coasts with contrasting modes of development. Hydrobia ventrosa is a direct developer that exchanges approximately 0.36 migrants per generation at this spatial scale. Considering the continuum between intermittent and episodic rafting routes, these populations may be sufficiently connected via rafting to prevent allopatric speciation but not local population differentiation. The species with planktonic development, H. ulvae, does not show a pattern of IBD and gene flow corresponds to 0.75 migrants every generation as inferred from genetic differentiation data, which led the authors to conclude that rafting is a possible means of LDD dispersal for the species (Wilke & Davis 2000). Finally, the bryozoan Membranipora membranacea with planktonic development shows low but detectable levels of gene flow (Nm = 0.09) at distances >10,000 km (Schwaninger 1999). Since 394

Figure 30 (A) Global distribution and sampling sites of the hydrozoan genus Obelia geniculata: JP – Japan, NZ – New Zealand, MA – Massachusetts, NB – New Brunswick, IC – Iceland, FR – France. (B) Haplotype network of mtDNA sequence data for populations of O. geniculata from the N Atlantic that shows that the Massachusetts population (MA) shares all haplotypes with New Brunswick (NB). (C) Phylogram based on same data for the populations of O. geniculata from Japan, New Zealand and the N Atlantic. This tree shows that within the N Atlantic many populations are paraphyletic (e.g., NB). Figures modified after Govindarajan et al. (2005).

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distances considered here are extremely large for larval dispersal, episodic rafting routes mediated on plastic substrata (Aliani & Molcard 2003) could account for the cosmopolitan distribution of the species and the low but persistent gene flow that prevents allopatric speciation. At this geographic scale and mostly toward 10,000 km, actual dispersal may be mostly humanmediated, but it cannot be excluded that rafting has occurred on isolated occasions in the evolutionary past. Rafting events may be so rare at this scale (e.g., one event every million years, episodic rafting routes) that populations have diverged significantly leading to allopatric speciation, and the observed genetic signals could be indicative of different species. Exemplifying this are the three deeply divergent clades (possibly cryptic species) of Obelia geniculata from Japan, New Zealand and the North Atlantic (Figure 30), which are thought to have originated >3 Mya. Rafting may have played a role in dispersing the ancestors of the populations from the different oceans (Govindarajan et al. 2005). Phylogeographic analysis of closely related species may be most suitable to reveal historic rafting events at this scale.

Gene flow patterns and contrasting developmental modes In general, brooders show higher levels of genetic differentiation among local populations than species with planktonic larval development (McMillan et al. 1992, Duffy 1993, Hunt 1993, Edmands & Potts 1997, Arndt & Smith 1998, Chambers et al. 1998, Todd et al. 1998, BoisselierDubayle & Gofas 1999, Kyle & Boulding 2000, Wilke & Davis 2000, Collin 2001, Andrade et al. 2003) (Figure 29). In situations where gene flow is indeed low for direct-developing species, they usually show increasing genetic isolation with increasing geographic distance (IBD) (e.g., Hellberg 1994, Ayre et al. 1997, Wilke & Davis 2000, Collin 2001, Goldson et al. 2001, Vianna et al. 2003). Several studies have compared genetic structure in taxa with different modes of development and have shown that sympatric sessile or semi-sessile species with contrasting modes of development often have similar genetic structure. Gene flow of sympatric species that are closely related (not necessarily congeners) may be constrained by similar dispersal barriers. The genetic differentiation values that have been reported among congeneric sympatric species with contrasting modes of development indicate that taxa with direct development generally display higher levels of genetic structure and IBD. Ayre et al. (1997) studied the genetic population structure of ascidians and corals from southeastern Australia, distinguishing solitary and colonial forms with high and limited dispersal potential, respectively. They found that solitary corals display little variation among local populations while local populations of colonial corals are highly differentiated. Comparison with data from other species inhabiting the same region confirmed their results (Hunt & Ayre 1989, Ayre et al. 1991, Hunt 1993, Billingham & Ayre 1996, Ayre et al. 1997, Hoskin 1997, Murray-Jones & Ayre 1997). The authors conclude that “even in a region where current flow is expected to be erratic, there is a clear contrast between the level of differentiation of broadcast-spawning and brooding species, and that for broadcast-spawning species the East Australian current is able to maintain high levels of gene flow and produce effectively panmictic breeding populations within the central and southern coasts of New South Wales” (Ayre et al. 1997). Particularly interesting are studies of congeners that differ in their dispersal potential based on developmental mode alone. Many of these studies conclude that direct-developing species have highly structured populations and a more robust pattern of IBD than species with planktonic larval development (see Table 2). Rafting can be invoked in cases where the phylogenetic and habitat characteristics of populations of species with contrasting modes of development are similar and the directly developing species lacks sufficient differentiation with respect to expectations (or does not fit an IBD pattern). For example, Ayre & Hughes (2000, 2004) have presented interesting results on the genetic divergence of populations of corals of the genus Acropora from the GBR in eastern Australia. In 396

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Table 2 Comparison of population genetic differentiation values among congeners with different modes of development Taxon

Genus

Anthozoa

Acropora

Acropora

Actinia

Pocillopora

Eucarida

Synalpheus

Prosobranchia

Cerithium

Crepidula Hydrobia

Littoraria

Littorina

Asteroidea

Patiriella

Echinoidea

Heliocidaris

Holothuroidea

Cucumaria

Ectoprocta (Bryozoa)

Alcyonidium

Direct development

Planktonic development

θ = *0.035 Nm = 6.89 1200 km FST = 0.29 Nm = 0.61 2400 km FST = 0.262 Nm = 2.33 1150 km θ = 0.15 Nm = 1.42 2400 km θ = 0.54 Nm = 0.21 4800 km FST = 0.58 Nm = 0.18 1750 km APV = *65.2 1300 km FST = 0.41 Nm = 0.36 6000 km FST = 0.185 Nm = 1.1 4000 km ΦST = *0.06 Nm = 3.9 3600 km FST = 0.462 Nm = 0.29 230 km GST = 0.62 Nm = 0.15 3400 km ΦST = 0.97 Nm = 0.01 2300 km FST = 0.077 Nm = 3 800 km

θ = *0.03 Nm = 8.08 1200 km FST = 0.21 Nm = 0.94 2500 km FST = 0.375 Nm = 0.42 1050 km θ = 0.056 Nm = 4.21 2000 km θ = 0.14 Nm = 1.54 4800 km FST = 0.158 Nm = 1.33 1750 km APV = –7.4 1300 km FST = 0.25 Nm = 0.75 6000 km FST = 0.028 Nm = 8.68 4000 km ΦST = *0.03 Nm = 8 250–750 km FST = 0.0008 Nm = 312.25 230 km GST = 0.12 Nm = 1.83 3400 km ΦST = 0.05 Nm = 4.75 2350 km FST = 0.105 Nm = 2.13 1500 km

Reference Ayre & Hughes 2000

Ayre & Hughes 2004

Ayre et al. 1991, Vianna et al. 2003

Ayre & Hughes 2004, Magalon et al. 2005

Duffy 1993

Boisselier-Dubayle & Gofas 1999

Collin 2001 Wilke & Davis 2000

Andrade et al. 2003

Kyle & Boulding 2000

Hunt 1993

McMillan et al. 1992

Arndt & Smith 1998

Porter et al. 2002

Notes: For each genus we present estimates of genetic differentiation among populations (or their averages) for species with differing modes of development at similar spatial scales. Nm values were calculated according to Wright (1969). Genera in bold indicate that the species with direct development has been inferred to raft. * Average value, details in Table 1.

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their first study conducted at a scale of 1200 km they found that species with both direct and planktonic larval development were effectively panmictic (Ayre & Hughes 2000). Indeed all studied species display low genetic differentiation and relatively high number of migrants per generation. Subsequently they expanded the geographic scale of their study and found that at a scale of 2400 km, species with direct and planktonic larval development show similar genetic differentiation (Ayre & Hughes 2004). The above results suggest that corals with different developmental modes in the GBR have similar realised dispersal distances and frequencies. Some coral species of the genus Acropora are known to raft on pumice (Jokiel 1990a), and even though it is not direct evidence that the species included in the genetic studies (Ayre & Hughes 2000, 2004) is a rafter, it is possible that rafting mediated connectivity prevents genetic differentiation among populations of the directdeveloping Acropora cuneata. Another example is provided by the comparison of the genetic differentiation in sea anemones provided by the studies of Vianna et al. (2003) and Ayre et al. (1991). They studied genetic differentiation in species of the genus Actinia with direct development from the coast of Bermuda and Brazil and with planktonic development from southeastern Australia, respectively. Interestingly, the direct-developing species displays lower genetic differentiation at a scale of 1150 km (Nm = 2.33) than the species with planktonic development at a similar scale (1050 km) (Nm = 0.42). Rafting has not been inferred for any of the two studied species of Actinia, but according to these data, the direct-developing Actinia bermudensis is achieving LDD by some means. Another example that involves greater gene flow for direct-developing species than for species with planktonic development is seen in bryozoans of the genus Alcyonidium, but opposed to the examples given above, the species with short-lived lecitotrophic larvae (restricted potential for autonomous dispersal), Alcyonidium gelatinosum, has the potential for rafting on algae (Porter et al. 2002). These authors found that bryozoan species from the British Isles with direct development have less genetic differentiation at a scale of 800 km (FST = 0.077) than bryozoans with planktonic larval dispersal at a scale of 1500 km (FST = 0.105), which is likely due to rafting-mediated connectivity for the species with short-lived larvae. Gastropods from the genus Littorina have been widely studied and compared with respect to their genetic structure and modes of development (Janson 1987a,b; Johannesson & Tatarenkov 1997; Johnson & Black 1998; Kyle & Boulding 2000; Andrade et al. 2003; Johannesson et al. 2004). Kyle & Boulding (2000) found that the direct-developing L. sitkana shows no genetic differentiation at the scale of >3000 km (FST = 0), and suggested that rafting has played an important role (see above). In general, species of Littorina that have planktonic larval development show similar or slightly less genetic differentiation at comparable scales than species with direct development. All the above leads to the conclusion that rafting is an important means of dispersal at different spatial scales and as previously emphasised, dispersal potential cannot be inferred from developmental mode alone. From small to large spatial scales, connectivity achieved through rafting (as reported above), matches closely the described rafting routes, from frequent, to intermittent and episodic.

Rafting dispersal and evolution Arrival in new habitats often leads to evolutionary change (Holt et al. 2005). This may be particularly true for species that have arrived on rafts as will be argued in the following subsections. One of the main differences between dispersal via rafting and planktonic larvae is that rafting, as opposed to larval dispersal, is usually not restricted to a particular ontogenetic stage. This may allow rafters to establish local populations during the rafting voyage (Thiel & Gutow 2005b). There are specific characteristics of the life history of many brooders that give additional evidence that they are particularly well adapted to colonise and persist after arriving in new habitats. Herein, genetic 398

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evidence will be reviewed that characterises the population structure of direct developers, and there will be discussion of the impact of rafting dispersal on (i) local recruitment and deme formation, (ii) colonisation across environmental gradients and (iii) the interplay between isolation and secondary admixture. Local recruitment and deme formation Rafting provides an effective means of dispersal for many brooders, particularly those that are likely to be found on floating substrata. Even though brooders may successfully achieve LDD through rafting, within a limited geographic area it has been observed that they show high levels of genetic differentiation (i.e., that they are highly microspatially structured) (Lessios et al. 1994, Johnson & Black 1995, Hoskin 1997). Organisms with direct development show distributions with greater patchiness than species with planktonic larval stages and within a patch they may contribute significantly to species diversity: “The fine scale spatial structure of direct-developing species was reflected in higher average species diversity within quadrats” (Johnson et al. 2001). Peracarids are common rafters and display life-history characteristics that may enhance their probabilities of successful dispersal through rafting. They brood their eggs up to a crawl-away stage and in many species offspring recruit in close proximity to their parents (Flach 1992, Thiel et al. 1997, Thiel 1999). In the marine environment, some peracarids may live in algae and have a relatively high potential for passive dispersal by rafting. Thiel & Vásquez (2000) found that algal holdfast communities are characterised by dense aggregations of single peracarid species that do not correlate with holdfast size, suggesting that local recruitment of these species occurred within the holdfast. Juveniles often excavate their galleries as offshoots of the maternal gallery (Menzies 1957, Jones 1971, Conlan & Chess 1992, Thiel 2003a), as a consequence of extended parental care (for review see Thiel 2003b). Consequently, populations of brooders often show differentiation at a microgeographic spatial scale. For example, the isopod Jaera albifrons shows differentiation over a scale of a few metres, consistent with deme formation (Piertney & Carvalho 1994, 1995; Carvalho & Piertney 1997). Similarly, Lessios et al. (1994) identified differentiation at the scale of hundreds of metres in the isopod Excirolana braziliensis, and populations of the amphipod Corophium volutator show significant differentiation within the Bay of Fundy (Wilson et al. 1997). Thus, peracarids often exhibit microscale genetic structure consistent with local recruitment resulting in deme formation. Johnson & Black (1995) studied the gene flow patterns in the brooding intertidal snail Bembicium vittatum in the Albrolhos Islands using direct and indirect methods. They found that along a continuous habitat there was a pattern of IBD that was absent in discontinuous habitats. Their results emphasise the importance of gene flow barriers on the genetic structure of species, particularly those with direct development. The recruitment pattern of these species, leading to deme formation within a microhabitat, could lead to high localised inbreeding (and potentially reduction in individual fitness) and divergence through genetic drift and localised selection (Piertney & Carvalho 1994, 1995). Deme formation appears to be common among species with direct development that inhabit patchy microhabitats (Piertney & Carvalho 1994, Sponer & Roy 2002, Colgan et al. 2005). However, Piertney & Carvalho 1995, found that the levels of genetic differentiation in Jaera albifrons resemble those found in other species with similar developmental modes that do not display deme formation, and thus, they concluded that “the ephemeral nature of some microhabitats may result in inbreeding being restricted to within one generation, reducing the overall effects of inbreeding depression and loss of heterozygosity in the localized population”. For brooders, local recruitment may represent an extreme advantage that enables them for LDD through rafting, as they may establish viable populations during the journey as well as during colonisation. In addition to local recruitment leading to deme formation, there are several other 399

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advantages that predispose direct developers for LDD; among the most important is their ability to disperse at any life stage (i.e., they are not restricted to the temporal duration of a particular ontogenetic stage in order to disperse). Transport and colonisation across environmental gradients On the microscale, rafting may occasionally transport organisms into habitats that are quite different from their native habitats. For example, this can happen across an intertidal gradient, where organisms from lower-shore habitats may be deposited on the higher shore. Due to their high colonisation potential, these rafting colonists may establish local populations, even in habitats with a new selective regime. Possibly this is occurring in species of Littorina from the North Pacific and North Atlantic, which are found both in the low and high intertidal zone. For the eastern North Atlantic, Panova & Johannesson (2004) reported divergent genetic adaptations between local populations of L. saxatilis from the lower and upper shore, which are in accordance with the respective selective pressures in either zone. Snyder & Gooch (1973) who studied this species in the western North Atlantic have discussed that “population isolation, with subsequent reduction in population size, promotes random drift and ultimate fixation of alleles. Shifting modes of natural selection over an ecologically heterogeneous area lead to genetic differences”. Based on ecological responses of L. saxatilis from the low and high intertidal zone, Pardo & Johnson (2005) also suggested that “selection may favour genotypes with low growth potential in lower zones and those with high growth potential in higher zones”. Cruz et al. (2004) suggested that divergence of ecotypes of L. saxatilis, which differ in size due to different selective environments, is enhanced by sizeassortative mating patterns. Sokolova & Boulding (2004) studied ‘ecotypes’ from the open shore and from salt marshes in two species of Littorina from the eastern North Pacific with consistent physiological differences. They suggested “that phenotypic differentiation in direct-developing species with limited dispersal is strongly affected by local adaptation and natural selection in heterogeneous habitats, and that strong local adaptation in the same type of habitat may result in convergent evolution producing superficially similar phenotypes”. At least one of the species they studied (L. sitkana) is also thought to disperse frequently via rafting (Behrens Yamada 1989, Kyle & Boulding 2000). Estevez (1994) reported isopods Sphaeroma terebrans, which usually bore into mangrove roots and wood, from rhizomes of saltmarsh plants. They suggested that isopods had arrived in the salt marsh on floating driftwood. Possibly, original founders colonised rhizomes due to lack of other suitable habitats. Nothing is known at present about the genetic relationship of rhizome populations and wood populations of S. terebrans. For the saltmarsh plant Elymus athericus, Bockelmann et al. (2003) also reported that withinsite populations from high and low shore differ more than between-site populations. They suggested “that markedly different selection regimes between these habitats, in particular intraspecific competition and herbivory, result in habitat adaptation and restricted gene flow over distances as small as 80 m”. Billard et al. (2005) revealed that Brittany populations of Fucus vesiculosus from the outer coast differed from those in bays. The authors suggested that this differentiation could be due to dispersal restrictions between bay and coastal populations. This is surprising since F. vesiculosus is probably the species from the genus Fucus, which is best adapted to float over considerable distances, and is commonly reported as floating in coastal waters of northwestern Europe (Tully & Ó Céidigh 1986, Davenport & Rees 1993, Franke et al. 1999, Vandendriessche et al., 2006). The possibility of differential selective pressures was not excluded by Billard et al. (2005): “Local population acclimation or adaptation to specific habitats causing lower establishment success between habitats cannot be ruled out as an additional explanation for this population differentiation”. 400

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The selective environments in the low and high intertidal zone or on the open shore and in sheltered bays are substantially different and this could result in genetic divergence of local populations across these gradients. For all of the species discussed above, rafting dispersal has been inferred or appears likely. However, why should these species be more prone to selective divergence across these gradients than other species? As mentioned above, rafting organisms have very little influence on selecting particular sites during the arrival process, and consequently they may be deposited over a wide range of ecological gradients. In contrast, planktonic larvae show diverse adaptations to select suitable habitats during settlement. They may settle only in a very restricted range across a gradient. Additionally, small, recently metamorphosed individuals may be highly susceptible to adverse environmental conditions. Rafting organisms, many of which feature direct development, release advanced developmental stages that may also survive in less favourable conditions. Consequently, rafters may initially survive over a wider range of environmental gradients than species with planktonic larvae. During subsequent population establishment, diverging selective pressures may result in genetic divergence of local populations, which is further enhanced by retention of lineages with favoured genes due to local recruitment of direct developers. Johannesson (2003) emphasised that: “The absence of pelagic larvae prevents rapid colonisation of habitats, but promotes local adaptation by subpopulations living generation after generation in the same habitat”. In her excellent review on evolutionary processes in littorinid snails she concluded that “we have evidence both from morphological and molecular traits that directional selection can produce rapid evolutionary changes. If such changes create reproductive barriers either directly or as secondary effects, reproductive isolation (and thus speciation) might appear more or less instantaneously upon an ecological shift of a population”. Interestingly, these rapid changes are most pronounced in those species with direct development, and rafting contributes to these microevolutionary processes. The interaction between rafting and direct development appears to play an important role in these processes, and it is suggested that future studies should a priori focus on this interaction. For species with planktonic larvae, Havenhand (1995) had stated: “Because the capacity for gene-flow between populations is frequently related to the dispersal potential of the larvae, the degree of larval dispersal may strongly mediate rates of evolution in marine species”. Rates of evolution in some rafting-dispersed direct developers may be particularly fast due to the reasons discussed. Isolation and secondary admixture As emphasised above, LDD via rafting may often result in isolated local populations. In particular in populations established on episodic rafting routes, periods of isolation may be sufficiently long to result in significant population divergence. There are abundant examples in the literature suggesting isolated dispersal events (see above) that resulted in allopatric speciation. For example, for littorinid snails, Williams et al. (2003) suggested dispersal of ancestors of recent species from the genus Austrolittorina in the Southern Ocean between New Zealand and South America about 15–30 Mya, and due to the long distance and intermediate larval lifetime they invoked rafting as a potential dispersal mechanism. Williams & Reid (2004) also suggested transatlantic dispersal in the equatorial current system starting around 20 Mya ago, when oceanic currents became stronger. They inferred that dispersal has primarily taken place in an easterly direction, but they did not discuss the dispersal mechanism. Based on the phylogeography of the species-rich genus Echinolittorina they emphasised that “speciation may be predominantly allopatric in each case, but on long coastlines allopatry is more likely to be transient, because of greater opportunities for postspeciation range extension, whereas geographical isolation should be more complete in island settings” (Williams & Reid 2004). Donald et al. (2005) inferred rafting events to have played an important role in the phylogenetic evolution of snails from the family Trochidae. In a phylogenetic 401

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analysis of marine bivalves from the genus Lasaea, Ó Foighil et al. (2001) also suggested that rafting followed by isolation has repeatedly influenced evolutionary processes. Rafting may also affect evolution in species with planktonic larvae. For example, Waters & Roy (2003) stated with respect to a widespread seastar genus with planktonic larval development “that both rare dispersal (e.g., rafting) and recent vicariance (e.g., formation of the Benguela Current) may have promoted allopatric divergence and speciation in Coscinasterias”. Rafting dispersal followed by isolation has also led to allopatric speciation in many terrestrial species. Most recent evidence comes from phylogenetic studies on reptiles. Carranza et al. (2000) inferred that geckos from the genus Neotarentula colonised Cuba up to 23 Mya, coming from North Africa, most likely rafting in the North Equatorial Current. Glor et al. (2005) reported that Caribbean species from the genus Anolis have diverged on different islands following overwater dispersal (via rafting). If isolation has not yet led to reproductive barriers, secondary contact via rafting may allow hybridisation of diverging clades. In general, founder effects, genetic bottlenecks, long periods of isolation and secondary admixture may result in a complex genetic pattern among local populations of many species. Possibly, the high degree of polymorphism among species commonly known as rafters is a consequence of various combinations of these processes. Occasional hybridisation between the different ecotypes of Littorina saxatilis may result in the observed polymorphism in this species (Pérez-Figueroa et al. 2005). Rafting may also allow exchange of similar ecotypes from different localities, further enhancing polymorphism in L. saxatilis. Another example might be found among the species of caprellid amphipods, which are commonly reported as rafters (Thiel & Gutow 2005b). Many of these species feature highly variable morphotypes (known as smooth and spinose forms). This group (and other peracarids) may prove in the future to be an excellent model to study evolutionary processes among common rafters with direct development. Evolutionary processes influenced by rafting represent an exciting challenge for marine biologists. Rafting-mediated evolution shows some particularities that are the result of the fact that this dispersal process usually transports a limited number of individuals, which nevertheless have a high likelihood of successfully establishing populations in new habitats. This increases the probability of founder effects and population persistence, even in isolation from other populations. While this may also increase the risk of extinction (due to inbreeding and low genetic diversity), there is ample indication that many founder populations have persisted and spread successfully in new habitats. Arrival of conspecifics (or congeners) long after the arrival of early colonists may lead either to secondary admixture or to sympatric coexistence of closely related species. In summary, evolutionary processes mediated by rafting can lead to species divergence, either in sympatry or in allopatry. Rafting thus contributes to local biodiversity, not only by importing colonisers to marine communities but also by facilitating speciation.

Implications for conservation of marine biodiversity Connectivity and conservation In accordance with conservation strategies applied in terrestrial systems, protected areas have been recognised as a powerful conservation tool in the marine environment also (Carr et al. 2003). Marine protected areas (MPA) and marine reserves are increasingly created in many regions of the world in order to provide refuges for over-exploited species or to protect biodiversity in general (Lubchenco et al. 2003, Palumbi 2004). Building on the metapopulation concept, it has been recognised that a single isolated MPA has only a limited potential for the protection of endangered species (Gerber et al. 2003). Isolated populations depend exclusively on local recruitment, making a population vulnerable to extinction if unpredictable climatic variations affect reproduction or survival (Figure 31). 402

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Sensitivity to local disturbance

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Local recruitment only

Local recruitment

Local recruitment

+

+

Larval immigration

Larval immigration

+ Rafting immigration

Openness of populations low

high

Figure 31 Relationship between the connectivity of local populations (via different mechanisms) and the sensitivity to disturbance. The openness or closed nature of populations makes them more or less dependent on local recruitment. Absolute dependence on local recruitment (closed population) leads to a high sensitivity to local disturbance, while populations open to the input of larval and/or rafting dispersal will be less sensitive to local disturbance.

Ensuring connectivity with other populations and immigration of propagules from other areas will alleviate failures in local recruitment and avoid extinctions of populations in an isolated reserve area. Consequently, networks of MPAs encompassing multiple local populations are required, because connected local populations are less vulnerable to local catastrophes (Figure 31). Resilience of a population to environmental changes can be expected to increase with the number of populations to which it is connected, because more connections result in a higher probability that at least some of the connections are not interrupted by environmental disturbances. Similarly, the larger the total area of a network, the higher is the probability that at least some of the local populations are not affected by local disturbances and maintain their function as a donor of individuals for affected populations (Allison et al. 2003, Halpern 2003). Rafting connections occur on a variety of spatial scales, and in particular those routes that connect local populations (frequent and intermittent rafting routes) need to be taken into account in the design of MPA networks. The major challenge in the development of MPA networks is the appropriate spacing of the subunits of a network in order to allow for sufficient connectivity between local populations (Shanks et al. 2003). Consequently, the creation of efficient MPA networks requires detailed knowledge of the dispersal capacities of the species under protection. To date, most efforts have focused on species with planktonic larvae (e.g., Guichard et al. 2004) and/or active migration (e.g., swimming) (e.g., Rakitin & Kramer 1996). Even though empirical data for dispersal distances of commonly rafting organisms are rare, there is growing indication that this might substantially contribute to the connectivity among local populations (see above). In many regions, rafting and other alternative dispersal mechanisms may contribute to the connectivity among populations that appeared to be 403

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unconnected when accounting only for larval dispersal or active migration. Considering all relevant aspects in the assessment of the dispersal capacity of a species (including the possibility of rafting) will allow for an accurate estimate of the connectivity of populations, the relative importance of local recruitment vs. immigration processes, and the vulnerability of a population toward environmental variability (see, e.g., Gerber et al. 2005). The development of efficient MPA networks requires a quantification of exchange processes of individuals between local populations. Even though complex behaviour (Yeung & Lee 2002) and physiological constraints of larvae (Anger 2003) complicate the modelling of dispersal, rafting dispersal is even more difficult to apprehend because it depends on multiple external variables and requires extensive empirical information from field investigations. The importance of external factors such as availability, quality, and longevity of rafts decreases the relative importance of intrinsic features of the organisms making exclusive laboratory investigations (as used for estimating the duration of larval development — see, e.g., Goffredo & Zaccanti 2004) insufficient in order to obtain reasonable estimates of rafting processes. The quantification of rafting opportunities and the assessment of the directionality of transport processes are basic aspects in the evaluation of the importance of rafting for the connectivity of populations in a given region. In addition to the extrinsic factors depending on currents and floating substrata, the life history of organisms needs to be taken into account. For many of the taxa that have been found on floating substrata, relatively little is known about their population connectivity (Table 3). For example, even though amphipods are among the most abundant rafting species, only for very few species are data available about population connectivity. Despite this general lack of knowledge about rafting organisms, it can be mentioned that many species feature particular life-history characteristics. Many common rafting species are small, have a limited reproductive potential (individual clutch sizes usually 40 km) from potential source populations. These examples demonstrate that artificial structures can serve as intermediate stepping stones, not only for species with planktonic larvae, but also for those that are thought to arrive as rafters. Anthropogenic structures may not only act as filters for floating substrata, but also as retention areas. For example, harbour basins often represent zones of reduced current velocities (Bulleri & Chapman 2004), where floating items might linger for longer time periods increasing the probability of successful disembarkation of associated rafters. In addition to their action in filtering out or retaining floating items, anthropogenic structures may also serve as important 408

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stepping stones, leading to a higher connectivity among local populations. In this context, Pinn et al. (2005) remarked that artificial hard substrata may “influence the dispersal of sessile organisms, allowing species that are poor dispersers to cover greater distances by using these structures as stepping stones” (see also Thompson et al. 2002). In general, human activities affect various stages of rafting journeys. Some activities may enhance connectivity between populations (introduction of plastics, construction of artificial filters and stepping stones), while others lead to a decreasing connectivity (retention of riverwood, elimination of filter habitats, coastline construction). Species that depend almost exclusively on rafting for dispersal can be expected to be most affected by these changes.

Outlook Some of the expressions most commonly used in this review are ‘may be’ or ‘suggest’. This demonstrates the high degree of uncertainty with respect to rafting as a dispersal process in the sea. However, the abundance of cases where authors are left with rafting as the only reasonable explanation for a certain pattern, is giving a clear signal. Rafting does occur and it connects populations of many species, or it transports organisms to new habitats where they may establish new populations. Based on the accumulated evidence the present authors believe that it is high time to move beyond the suggestive phase. Rafting plays an important role over most spatial and temporal scales operating in present-day oceans. The urgent need for effective and representative conservation measures in the marine environment requires that rafting be taken into account. The directionality of rafting dispersal, similar to the situation for larval dispersal, is crucial for the spatial arrangement of marine reserve networks. Accordingly, marine network reserves need to consider connectivity including rafting-mediated dispersal, which requires understanding the rafting dynamics of marine metapopulations (i.e., source-sink dynamics, sources of floating substrata). For example, if populations persist in a source-sink system with down-current sink populations being supplied from a large up-current source population, it is important to define adequate up-current reserve areas. The up-current area must not only provide supply of individuals but also sufficient rafts necessary for appropriate transport of organisms. The identification of relevant natural raft sources such as macroalgal belts, mangrove forests, salt marshes, or seagrass beds (see above) are, thus, obligatory for the development of efficient management programmes. Recognition of source areas might be complicated when rafts originate from distant sources without any obvious spatial relation to the actual conservation area. Rafts themselves (or the rafting organisms) may carry signals that allow the identification of source areas. Jokiel (1989), for example, collected rafting colonies of corals from floating pumice at Hawaii: the chemical composition of pumice can be utilised to identify source regions (Frick & Kent 1984, Jokiel & Cox 2003). Other characteristics of floating items (or size of rafting organisms) could also be used to infer their origin. Some of the most powerful tools to identify potential source regions are the genetic signals of the organisms themselves as has been demonstrated by several of the studies presented herein. Rafting not only poses challenges to conservation biologists, it also offers opportunities. One of the main questions in the study of marine reserve design is the question for source and sink regions: where do the organisms living in a marine reserve actually come from? Also one of the principal questions related to rafters observed on the high seas (or arriving in coastal habitats) is, where do they come from? Rafters can be traced back to the source regions by a variety of methods (see above). However, in contrast to tiny planktonic larvae, where evidence for source regions usually is inferential (e.g., Becker et al. 2005, Zacherl 2005), rafts can also be followed at sea and tracked during the rafting journey. Following dispersing organisms would also provide an understanding of the processes leading to the survival or demise of rafters. In a previous review (Thiel & Gutow 2005b), it was argued that long-distance rafters may reproduce during the journey, and in 409

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the present review it is suggested that this may lead to founder effects within rafts. These processes may also influence the viability and genetic structure of groups of colonisers in new habitats. In order to understand these processes satisfactorily it is necessary not only to examine populations in source and sink regions, but also groups of travellers. It is therefore suggested that molecular studies that examine the population connectivity of coastal organisms should also incorporate rafting individuals whenever possible and feasible. It appears that the study by Reusch (2002) is the only one that sampled rafting individuals in an attempt to identify their source of origin with the aid of molecular markers. While rafting on the one hand offers unique opportunities in tracking organisms, on the other hand, direct testimony of arrival is much less likely than for species with planktonic larvae. Numerous studies have examined settlement in planktonic larvae, and many more have monitored recruitment events (for synthesis see, e.g., Eckert 2003). In contrast, very few investigators were actually present during the arrival of rafters. Successful colonisations by rafters are often only detected a long time after the arrival event. This is not very different from the arrival of species transported by other dispersal agents (e.g., birds, fish or humans). In these cases, the appearance of invaders often is noticed many years or decades after the first arrival. Not surprisingly, very little is known about the arrival process and initial colonisation in both categories. Consequently, in many cases it is difficult to infer whether an organism has arrived in a new area via rafting or via other agent-mediated transport mechanisms. Molecular studies can help to answer this question, because they permit an estimation of whether arrival has happened very recently or far back in time. For example, in a series of studies Duran et al. (2004a,b,c) have examined the present geographic distribution of the marine sponge Crambe crambe (which has short-lived lecitotrophic larvae) around the coasts of the Mediterranean and the North Atlantic (Madeira and Canary islands). At a scale of 3000 km, Duran et al. (2004a,b) found high genetic structure of populations following an IBD pattern based on microsatellites and nuclear DNA. The shallow divergence among sequence types in this study, led the authors to propose that C. crambe either is a young species (with no time to generate large sequence divergence) or an old species that has suffered demographic changes or a low mutation rate (Duran et al. 2004b). Duran et al. (2004b) elaborated on potential demographic changes as being “a strong recent bottleneck that has reduced its former genetic diversity, followed by a new expansion and accumulation of new mutations”. The authors offered human-mediated dispersal as the most likely explanation for recent exchange among populations of C. crambe, but they did not completely discount rafting as a possibility, which could result in a similar genetic pattern. Molecular studies have also helped to reveal that the present-day distribution of many organisms is due to historic dispersal events, most likely via rafting. In the wake of these studies it has been increasingly recognised that rafting may have contributed significantly to the species succession and biodiversity of coastal ecosystems and island communities. More species may have reached these habitats via rafting than previously assumed. For example, in an extensive review (Thiel & Gutow 2005b) reported a total of 17 invertebrate species for which rafting was inferred based on genetic data. Twelve of these species have never been observed on or near a raft, but based on all available evidence the authors of the respective studies offered rafting as the most probable explanation for the observed genetic patterns. It is likely that in the future the number of species for which rafting is inferred based on genetic evidence will be increasing. Extensive evidence has been provided that rafting is an important mechanism that affects biodiversity at a local and global level. From frequent to episodic rafting routes there exists a continuum of rafting intensity, distance and selective pressures (= filters) posed to rafters, which influences processes from population dynamics to allopatric speciation. It has been shown that different rafting routes provide varying degrees of connectivity for populations. Also, that organisms with direct development can achieve LDD via rafting and that the Rockall Paradox is no longer a

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paradox. Based on the evidence and examples presented herein, it becomes clear that raftingmediated dispersal of organisms is yet another process that needs to be taken into account when studying and interpreting the biogeography and evolution of coastal organisms.

Acknowledgements This final part of a series of reviews on the ecology of rafting was originally planned and designed together with Lars Gutow. For work-related reasons Lars finally could not be part of this endeavour. He has contributed enormously to our ideas and concepts about rafting and we are extremely thankful for his unconditional support. Christian Buschbaum, Larry Harris, Irv Kornfield and Peter Smith accepted the challenge to read large parts or the entire version of a preliminary draft. Their thoughtful and constructive comments are deeply appreciated. This manuscript would not have seen the light of day without the enormous help of Ivan Hinojosa who shepherded the literature and of Erasmo Macaya who skilfully prepared many of the figures. We thank them whole-heartedly for their efforts. Any mistakes or misinterpretations are entirely our own responsibility. Funding during the writing of this manuscript was through FONDECYT 1010356 (MT) and 1051076 (PH, MT). MT once more acknowledges a generous invitation by the Alfred Wegener Institute for Polar and Marine Research during the writing phase of this review.

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Oceanography and Marine Biology: An Annual Review, 2006, 44, 431-464 © R. N. Gibson, R. J. A. Atkinson, and J. D. M. Gordon, Editors Taylor & Francis

POTENTIAL EFFECTS OF CLIMATE CHANGE ON MARINE MAMMALS J.A. LEARMONTH1, C.D. MACLEOD1, M.B. SANTOS1,2, G.J. PIERCE1, H.Q.P. CRICK3 & R.A. ROBINSON3 1School of Biological Sciences [Zoology], University of Aberdeen, Tillydrone Avenue, Aberdeen, AB24 2TZ, U.K. E-mail: [email protected] 2Instituto Español de Oceanografía, Centro Costero de Vigo, Cabo Estay, Canido, 36200 Vigo, Spain 3British Trust for Ornithology, The Nunnery, Thetford, IP24 2PU, U.K.

Abstract Predicted impacts of climate change on the marine environment include an increase in temperature, a rise in sea levels and a decrease in sea-ice cover. These impacts will occur at local, regional and larger scales. The potential impacts of climate change on marine mammals can be direct, such as the effects of reduced sea ice and rising sea levels on seal haul-out sites, or species tracking a specific range of water temperatures in which they can physically survive. Indirect effects of climate change include changes in prey availability affecting distribution, abundance and migration patterns, community structure, susceptibility to disease and contaminants. Ultimately, these will impact on the reproductive success and survival of marine mammals and, hence, have consequences for populations. Marine mammal species, which have restricted geographical distributions with little or no opportunity for range expansion in response to climate change, may be particularly vulnerable to the effects of climate change. The potential effects of climate change on marine mammals have a number of implications for their conservation and highlight several areas requiring further research.

Introduction The Earth’s climate is changing (IPCC 2001a). The global average land and sea surface temperature has increased over the twentieth century and precipitation has increased over the same period, particularly over mid- and high-latitudes. These changes have had secondary impacts. For example, as temperatures have increased the extent of ice cover has decreased and global sea level has risen. Such changes are evident from the global network of climate instruments and, over a longer timescale, from the use of historical proxies such as tree rings or ice cores. The causes of such changes are open to debate, but most of the observed warming over the last 50 yr has probably been due to increased CO2 emissions, and these increases are likely to continue (e.g., Hulme et al. 2002, EEA 2004). Global climate change will affect the physical, biological and biogeochemical characteristics of the oceans and coasts. Known or predicted large-scale and regional impacts of climate change on the marine environment include an increase in temperature, a rise in sea levels, and changes in ocean circulation, sea-ice cover, salinity, CO2 concentrations, pH, rainfall patterns, storm frequency, wind speed, wave conditions and climate patterns (FRS 1998, Hansen et al. 2001, IPCC 2001a, Sear et al. 2001, Hulme et al. 2002, FRS 2003, ICES 2004). 431

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Climate change is likely to present a major challenge to the world’s wildlife, and to impact overall levels of biodiversity. Changing climate has already had a number of impacts on wildlife, across a range of taxa, and these impacts are set to increase unless suitable mitigation measures are taken (Walther et al. 2002, Parmesan & Yohe 2003, Root et al. 2003, EEA 2004, Parmesan & Galbraith 2004). The effect of climate change on the marine environment has the potential to have, and in some cases has already had, a considerable impact on marine ecosystems and species. These effects could include changes in abundance, distribution, timing and range of migration, community structure, the presence and species composition of competitors and/or predators, prey availability and distribution, timing of breeding, reproductive success and, ultimately, survival (IWC 1997, Tynan & DeMaster 1997, Harwood 2001, Würsig et al. 2002). While some species may increase in abundance or range, climate change will increase the risk of extinction of other more vulnerable species. The geographical extent of the damage or loss, and the number of systems affected, will increase with the magnitude and rate of climate change (IPCC 2001a). Uncertainties about the nature and degree of future climate change make it impossible to know exactly how weather, ocean circulation and biological productivity will be affected (for example, Weaver & Zwiers 2000). Effects on the marine environment are especially difficult to predict because of the complex interactions between ocean processes and climate and will vary greatly between areas. Therefore, predictions of the effects on species and populations are highly speculative (Würsig et al. 2002). The impacts of climate change will reflect the timing and geographic scale of the changes, as well as on the longevity, generation time and geographic distribution of the species (Würsig et al. 2002). For example, large but ‘slow’ (in the order of decades or centuries) shifts in the climate have occurred throughout the Earth’s history, and these have driven the evolution of adaptive characteristics, within-species variations, population discreteness and extinctions (Würsig et al. 2002). There have been several recent papers linking the effects of climate change to marine mammals (e.g., Ferguson et al. 2005, MacLeod et al. 2005). The present paper reviews current information on the observed and predicted changes in climate and their potential impacts, direct and indirect, on marine mammals. Examples of observed effects are given for mysticetes (baleen whales), odontocetes (toothed whales, dolphins and porpoises), pinnipeds (seals, sea lions and walruses), sirenians (manatee and dugong) and the polar bear (Ursus maritimus), based on published accounts and reports. Many of the indirect effects of climate change on marine mammals will be through changes in prey availability; therefore potential effects of climate change on prey species, such as fish, cephalopods and plankton are also reviewed.

Range of marine mammals Marine mammals are found in just about all ocean habitats, as well as several rivers and inland seas. In the open ocean, marine mammals may be thought of as ‘surface dwellers’, that spend most of their lives within about 200 m of the surface, ‘deep divers’, that routinely dive to depths below 500 m for short periods of time, or ‘deep dwellers’ that spend much of their time at depths below 500 m. Several species are semipelagic; occurring in areas between shallow and deep water, often at the edge of the continental shelf or some other underwater feature. Many marine mammals are coastal, with baleen whales, odontocetes, pinnipeds and sirenians all having coastal representatives (Würsig 2002). A species’ distribution is affected by a combination of demographic, evolutionary, ecological, habitat-related and anthropogenic factors although, in general, prey availability is likely to be particularly critical (Forcada 2002). Species habitat preferences are generally thought to be related to the distribution of preferred prey, which in turn are often determined by physical oceanographic features. Therefore, the habitat preferences of marine mammals are often defined by physical and chemical characteristics of the water, which define water masses and current boundaries where 432

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prey accumulates. For example some species, such as Heaviside’s (Cephalorhynchus heavisidii), Commerson’s (C. commersonii) and Peale’s (Lagenorhynchus australis) dolphins, are associated with cold-water currents, and blue whales (Balaenoptera musculus) are often found in areas of cool upwelling waters (Forcada 2002, LeDuc 2002). Therefore, although marine mammals are observed widely across the world’s oceans, distribution within the overall range is often patchy, with some areas being used more frequently than others. These ‘preferred’ areas or ‘critical habitats’ are probably particularly important for survival and reproduction, and it is changes to these areas that are most likely to affect the distribution and abundance of marine mammals (Harwood 2001). While the fine-scale distribution of marine mammal species may be related to oceanographic features and conditions through their effects on prey distribution, the regional or global ranges of marine mammal species are often related to water temperature (Table 1). For example, bowhead whales (Balaena mysticetus) and narwhals (Monodon monoceros) are found only in Arctic waters, Atlantic white-beaked dolphins (Lagenorhynchus albirostris) are only found in cold temperate waters, and species such as spinner (Stenella longirostris) and pantropical spotted (S. attenuata) dolphins are restricted to tropical waters (Mann et al. 2000). A species’ range may be limited in some cases because it is not adapted for living in certain environments. For example, tropical delphinids may not range into higher latitudes due to limitations on their abilities to thermoregulate in colder water or find food in different habitats. Competition, either from closely related species or from ecologically similar species, may also exclude a species from a particular region in which it could otherwise survive (i.e., competitive exclusion) (Forcada 2002). However, whether the relationship between the range of many marine mammal species and water temperature is direct, with species only being able to survive within specific temperature ranges, or indirect with temperature affecting competitive abilities of ecologically similar species, is unknown in most cases. Within a species range, there may be regular changes in areas of occurrence as their biological and ecological requirements change (Forcada 2002). Of these changes, the most common are seasonal migrations. Migration can be described as “the seasonal movement between two geographic locations that is related to the reproductive cycle, changes in temperature, and prey availability” (Forcada 2002) or “the persistent movement between two destinations” (Cockeron & Connor 1999). The Bonn Convention on the Conservation of Migratory Species of Wild Animals (1979) (CMS) is an important instrument in the management of migratory species. It defines a migratory species as “the entire population or any geographically separate part of the population of any species or lower taxon of wild animals, a significant proportion of whose members cyclically and predictably cross one or more national jurisdictional boundaries”. The basic driving forces for migration are ecological and biogeographic factors, like seasonality, spatiotemporal distributions of resources, habitats, predation and competition (Alerstam et al. 2003). The triggers for migration may relate to changes in day length but, as the timing of migrations can vary from year to year, prey abundance may also be an important factor, and temperature and seaice formation can also be influential (Stern 2002). Most baleen whales (mysticetes), such as blue, grey (Eschrichtius robustus), fin (Balaenoptera physalus), sei (B. borealis), northern and southern right whales (Balaena glacialis and B. australis) and humpback whales (Megaptera novaeangliae), undertake long seasonal migrations between tropical calving grounds in winter and high latitude feeding grounds in summer. For example, grey whales are highly migratory with an annual migration covering up to 15,000–20,000 km between summer feeding grounds in Arctic or subarctic waters and winter breeding grounds in temperate or subtropical southern waters (Jones & Swartz 2002). Bowhead whales also migrate but their longitudinal movements are equal to or greater than their latitudinal movements and they never leave Arctic waters. The migration or seasonal movements of Bryde’s (Balaenoptera edeni) and minke whales (B. acutorostrata) are often less well defined and less predictable than those of other migratory baleen whales (Forcada 2002). 433

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Table 1 Species range (breeding site for pinnipeds), IUCN status and potential effects of climate change on the range of cetaceans, pinnipeds, sirenians and other marine mammal species Family and species name

Common name

Mysticeti

Baleen Whales

Balaenidae Balaena mysticetus

Bowhead whale

Balaena glacialis Balaena australis

Northern right whale Southern right whale

Potential effects of climate change on species range

Species range (breeding site for pinnipeds)

IUCN status

N Hemisphere: Arctic waters, circumpolar N Atlantic & Pacific: subpolar to tropical S Hemisphere: Antarctic to temperate

LR:cd

↓

EN (D)

?↓

LR:cd

?↓

Neobalaenidae Caperea marginata

Pygmy right whale

S Hemisphere: circumpolar, cold temperate

Eschrichtiidae Eschrichtius robustus

Grey whale

N Pacific: warm temperate to arctic

LR:cd

?

Balaenopteridae Megaptera novaeangliae

Humpback whale

Worldwide: cold temperate/polar to tropical Worldwide: polar to tropical S Hemisphere: polar to tropical

VA (A)

?

LR:nt LR:cd

? ?

Balaenoptera edeni/brydei

Minke whale1 Antarctic minke whale1 Bryde’s whale

Balaenoptera borealis

Sei whale

Balaenoptera physalus Balaenoptera musculus

Fin whale Blue whale

Odontoceti Physeteridae Physeter macrocephalus

Toothed Whales

Balaenoptera acutorostrata Balaenoptera bonaerensis

Kogiidae Kogia breviceps Kogia sima

Ziphiidae Ziphius cavirostris Berardius arnuxii Berardius bairdii

Worldwide: tropical Worldwide: tropical Worldwide: Worldwide:

?↓

warm temperate to

DD

cold temperate to

EN (A)

?

polar to tropical polar to tropical

EN (A) EN (A)

? ?

Sperm whale

Worldwide: polar to tropical

VU (A)

?

Pygmy sperm whale Dwarf sperm whale

Worldwide: warm temperate to tropical Worldwide: warm temperate to tropical

DD

↑

Cuvier’s beaked whale Arnoux’s beaked whale Baird’s beaked whale

Worldwide: cold temperate to tropical S Hemisphere: circumpolar, polar to subtropical N Pacific: polar to subtropical

DD

?

LR:cd

?

LR:cd

?

434

↑

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Table 1 (continued) Species range (breeding site for pinnipeds), IUCN status and potential effects of climate change on the range of cetaceans, pinnipeds, sirenians and other marine mammal species Family and species name Tasmacetus shepherdi Indopacetus pacificus Hyperoodon ampullatus Hyperoodon planiforms Mesoplodon hectori Mesoplodon mirus Mesoplodon europaeus Mesoplodon bidens Mesoplodon grayi Mesoplodon peruvianus Mesoplodon bowdoini Mesoplodon carlhubbsi Mesoplodon ginkgodens Mesoplodon stejnegeri Mesoplodon layardii Mesoplodon densirostris Mesoplodon traversii Mesoplodon perrini

Platanistidae Platanista gangetica

Iniidae Inia geoffrensis

Potential effects of climate change on species range

Common name

Species range (breeding site for pinnipeds)

IUCN status

Shepherd’s beaked whale Longman’s beaked whale Northern bottlenose whale Southern bottlenose whale Hector’s beaked whale True’s beaked whale Gervais’ beaked whale Sowerby’s beaked whale Gray’s beaked whale Pygmy beaked whale Andrew’s beaked whale Hubbs’ beaked whale Ginko-toothed beaked whale Stejneger’s beaked whale Strap-toothed beaked whale Blainville’s beaked whale Spade-toothed whale Perrin’s beaked whale

S Hemisphere: warm temperate to subpolar Indian Ocean and Pacific: tropical waters N Atlantic: arctic to cold temperate waters S Hemisphere: circumpolar, Antarctic to temperate S Hemisphere: cold temperate to subtropical Worldwide: warm temperate to subtropical Atlantic: warm temperate to tropical N Atlantic: subpolar to warm temperate S Hemisphere: cold to warm temperate SE and NE Pacific: cold temperate to tropical S Hemisphere: cold temperate to subtropical N Pacific: cold temperate to subtropical N Pacific and Indian Ocean: temperate to tropical N Pacific: warm temperate to subpolar S Hemisphere: polar to subtropical Worldwide: warm temperate to tropical Unknown possibly S Pacific: cold temperate to subtropical Unknown possibly NE Pacific: warm temperate to subtropical

DD

?

DD

?

LR:cd

↓

LR:cd

?

DD

?

DD

?↑

DD

?↑

DD

?

DD

?

DD

?

DD

?

DD

?

DD

?

DD

?

DD

?

DD

?

Ganges river dolphin

India, Nepal, Bhutan and Bangladesh: freshwater only

EN (A)

↓

Boto

Peru, Ecuador, Brazil, Bolivia, Venézuela, Colombia: freshwater only

VU (A)

↓

435

?↑ ?

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Table 1 (continued) Species range (breeding site for pinnipeds), IUCN status and potential effects of climate change on the range of cetaceans, pinnipeds, sirenians and other marine mammal species Family and species name

Potential effects of climate change on species range

Common name

Species range (breeding site for pinnipeds)

IUCN status

Lipotidae Lipotes vexillifer

Baiji

China: freshwater only

CR (ACD)

↓

Pontoporiidae Pontoporia blainvillei

Franciscana

Brazil to Argentina: coastal waters from Doce River

DD

↓

Circumpolar in arctic seas: arctic to cold temperate Arctic Ocean

VU (A)

↓

Monodon monoceros

Beluga or white whale Narwhal

DD

↓

Delphinidae Cephalorhynchus commersonii

Commerson’s dolphin

DD

↓

Cephalorhynchus eutropia

Chilean dolphin

DD

?

Cephalorhynchus heavisidii

Heaviside’s dolphin Hector’s dolphin

S America, Falkland and Kerguelen islands: coastal, subpolar to cold temperate S South America: coastal, subpolar to warm temperate SW Africa: cold to warm temperate New Zealand: coastal waters, cold to warm temperate Worldwide: warm temperate to tropical SE Atlantic: coastal and river mouths, subtropical to tropical Indian Ocean: coastal, subtropical to tropical Indian Ocean: coastal and rivers, tropical SW Atlantic: coastal, estuaries and rivers, tropical Indian and Pacific Ocean: coastal, tropical Worldwide: cold temperate to tropical Worldwide: tropical

DD

?

EN (AC) DD

↓

DD

?

Monodontidae Delphinapterus leucas

Cephalorhynchus hectori Steno bredanensis

Sotalia fluviatilis

Rough-toothed dolphin Atlantic humpbacked dolphin Indian humpbacked dolphin Indo-pacific humpbacked dolphin Tucuxi

Tursiops aduncus

Bottlenose dolphin

Tursiops truncatus

Bottlenose dolphin

Stenella attenuata

Pantropical spotted dolphin Atlantic spotted dolphin Spinner dolphin Clymene dolphin Striped dolphin

Sousa teuszii Sousa plumbea Sousa chinensis

Stenella frontalis Stenella longirostris Stenella clymene Stenella coeruleoalba

Atlantic Ocean: subtropical to tropical Worldwide: tropical Atlantic Ocean: tropical Worldwide: cold temperate to tropical

436

?

? DD

?

DD

↓

DD

?

DD

↑

LR:cd

?↑

DD

?↑

LR:cd DD LR:cd

?↑ ? ?↑

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POTENTIAL EFFECTS OF CLIMATE CHANGE ON MARINE MAMMALS

Table 1 (continued) Species range (breeding site for pinnipeds), IUCN status and potential effects of climate change on the range of cetaceans, pinnipeds, sirenians and other marine mammal species Family and species name Delphinus delphis Delphinus capensis Delphinus tropicalis Lagenodelphis hosei Lagenorhynchus albirostris

Common name Short-beaked common dolphin2 Long-beaked common dolphin2 Arabian common dolphin2 Fraser’s dolphin

Lagenorhynchus obliquidens Lagenorhynchus obscurus

White-beaked dolphin Atlantic whitesided dolphin Pacific white-sided dolphin Dusky dolphin

Lagenorhynchus australis

Peale’s dolphin

Lagenorhynchus cruiger

Hourglass dolphin

Lissodelphis borealis

N. right whale dolphin S. right whale dolphin Risso’s dolphin

Lagenorhynchus acutus

Lissodelphis peronii Grampus griseus Peponocephala electra Feresa attenuata

Melon-headed whale Pygmy killer whale

Pseudorca crassidens

False killer whale

Orcinus orca Globicephala melas Globicephala macrorhynchus Orcaella brevirostris

Killer whale, orca Long-finned pilot whale Short-finned pilot whale Irrawaddy dolphin

Phocoenidae Neophocaena phocaenoides

Finless porpoise

Phocoena phocoena

Harbour porpoise

Species range (breeding site for pinnipeds)

IUCN status

?↑

Worldwide: temperate and tropical Worldwide: subtropical Arabian Sea: coastal waters, tropical Worldwide: warm temperate to tropical N Atlantic: cold temperate N Atlantic: subpolar to warm temperate N Pacific: cold temperate to subtropical S Hemisphere: cold to warm temperate S America: subpolar to warm temperate S Hemisphere: polar to warm temperate N Pacific: subpolar to subtropical S Hemisphere: polar to subtropical Worldwide: cold temperate to tropical Worldwide: tropical Worldwide: tropical to warm temperate Worldwide: warm temperate to tropical Worldwide: polar to tropical Worldwide (ex N Pacific): polar to warm temperate Worldwide: tropical to subtropical SE Asia, N Australia and Papua New Guinea: tropical coastal waters and estuaries

Indo-Pacific: warm temperate to tropical N Pacific and N Atlantic: subpolar to cold temperate

437

Potential effects of climate change on species range

?↑ ? DD

?↑

?↓ ?↓ DD

?↓

DD

? ?↓ ?

DD

?

DD

? ?↑ ?↑ ?↑

LR:cd

? ?

LR:cd

?↑

DD

↓

DD

?

VU (A)

?↓

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Table 1 (continued) Species range (breeding site for pinnipeds), IUCN status and potential effects of climate change on the range of cetaceans, pinnipeds, sirenians and other marine mammal species Family and species name

Potential effects of climate change on species range

Common name

Species range (breeding site for pinnipeds)

IUCN status

Gulf of California: subtropical S America: coastal cold temperate to subtropical S Hemisphere: polar to cold temperate N Pacific: subpolar to temperate

CR (C) DD

↓ ?

DD

?↓

Phocoenoides dalli

Vaquita Burmeister porpoise Spectacled porpoise Dall’s porpoise

LR:cd

?

Otariidae Artocephalus pusillus

Cape fur seal

Artocephalus gazelle

Antarctic fur seal

Artocephalus tropicalis

Subantarctic fur seal Guadalupe fur sea

Phocoena sinus Phocoena spinipinnis Phocoena dioptrica

Zalophus californianus

California sea lion

Zalophus wollebaeki

Galápagos sea lion

Eumetopias jubatus

Steller sea lion

Neophoca cinera

Australian sea lion

Phocarctos hookeri

New Zealand sea lion South American sea lion

S Africa and S Australia: warm temperate (land) S Hemisphere (excluding SE Pacific): polar to subpolar S Hemisphere (excluding SE Pacific): high temperate NE Pacific: warm temperate to tropical (land) West coast of South America, Chile: temperate (land) S Australia and New Zealand: temperate (land) S America and Falklands: subpolar to temperate (land) Galápagos Islands: equatorial (land) N Pacific and Bering Sea: subpolar to temperate (land) NE Pacific: warm temperate to tropical (land) Galápagos Islands: equatorial (land) N Pacific: subpolar to cold temperate (land) SE Indian Ocean, S and SW Australia: temperate (land) SW Pacific, NZ: subpolar to cold temperate (land) S America and Falklands: polar to subtropical (land)

Odobenidae Odobenus rosmarus

Walrus

Arctic Ocean and adjoining seas

?↓

Phocidae Ergnathus barbatus Phoca vitulina

Bearded seal Harbour seal

Arctic (pack ice) N Hemisphere: subpolar to warm temperate (land)

?↓ ?

Artocephalus townsendi Artocephalus philippii Artocephalus forsteri Artocephalus australis Artocephalus galapagoensis Callorhinus ursinus

Otaria flavescens

Juan Fernández furseal New Zealand fur seal South American fur seal Galápagos fur seal Northern fur seal

438

? ?↓ ? VU (D)

?

VU (D)

? ? ?

VU (A)

?↓

VU (A)

? ?

VU (A)

?↓

EN (A)

?↓ ?

VU (D)

? ?

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Table 1 (continued) Species range (breeding site for pinnipeds), IUCN status and potential effects of climate change on the range of cetaceans, pinnipeds, sirenians and other marine mammal species Family and species name

Common name

Phoca largha

Spotted seal

Pusa hispida

Ringed seal

Pusa caspica

Caspian seal

Pusa sibirica

Baikal seal

Halichoerus grypus

Grey seal

Histriophoca fasciata Pagophilus groenlandicus

Ribbon seal Harp seal

Cystophora cristata

Hooded seal

Monachus monachus

Mediterranean monk seal

Monachus schauinslandi

Leptonychotes weddellii Ommatophoca rossii Lobodon carcinophaga Hydrurga leptonyx

Hawaiian monk seal Southern elephant seal Northern elephant seal Weddell seal Ross seal Crabeater seal Leopard seal

Trichechidae Trichechus manatus

Caribbean manatee

T. m. latirostris

Florida manatee

T. m. manatus

Antillean manatee

Trichechus senegalensis

African manatee

Trichechus inunguis

Amazon manatee

Dugongidae Dugong dugon

Dugong

Mirounga leonina Mirounga angustirostris

Species range (breeding site for pinnipeds) N Pacific, Chukchi Sea: polar (pack ice) Arctic regions, Baltic Sea: (fast ice) Caspian Sea: polar to subpolar (fast ice) Lake Baikal, Siberia: polar to subpolar (fast ice) N Atlantic: subpolar to cold temperate (land, ice) N Pacific: polar (pack ice) N Atlantic: polar to cold temperate (pack ice) N Atlantic: polar to cold temperate (pack ice) Med. Sea, Black Sea, NW African coast: subtropical (land) Hawaiian Islands: tropical (land)

IUCN status

Potential effects of climate change on species range ?↓ ?↓

VU (B)

?↓

LR:nt

?↓ ?↓ ?↓ ?↓ ?↓

CR (C)

?↓

EN (C)

?

Subantarctic, Antarctic, southern S. America (land) N Pacific: subpolar to subtropical (land) Antarctic (fast ice) Antarctic (fast ice) Antarctic (pack ice) Antarctic (pack ice)

?↓ ?↓ ?↓ ?↓ ?↓ ?

Florida, Caribbean (marine and freshwater) Florida peninsula, occasionally as far south as Bahamas Mainland coast from Mexico to Venezuela, and Brazil including the Greater and Lesser Antilles West Africa (marine and freshwater) Amazon river (marine and freshwater)

VU (A)

?↑

VU (A)

?

VU (A)

?

Indian and western Pacific oceans (marine)

VU (A)

?

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Table 1 (continued) Species range (breeding site for pinnipeds), IUCN status and potential effects of climate change on the range of cetaceans, pinnipeds, sirenians and other marine mammal species Family and species name

Potential effects of climate change on species range

Common name

Species range (breeding site for pinnipeds)

IUCN status

Ursidae Ursus maritimus

Polar bear

Arctic

LR:cd

?↓

Mustelidae Enhydra lutris

Sea otter

EN (A)

?

Lontra felina

Marine otter

EN (A)

?

Lutra lutra

Common otter

Canada, U.S., Mexico, Japan, Russian Federation (terrestrial, marine) Argentina, Chile, Peru (terrestrial, freshwater, marine) Worldwide (terrestrial, freshwater, marine)

NT

?

Notes: ↑ indicates a possible increase in range, ↓ indicates a possible decrease in range and ? indicates effects on range are unknown. IUCN status: (CR = critically endangered; EN = endangered; VU = vulnerable; A = declining population, B = small distribution and decline or fluctuation, C = small population size and decline, D = very small or restricted); NT = near threatened; LR:cd = low risk, conservation dependent; LR:nt = low risk, near threatened; DD = data deficient. 1. Minke whale: several authors refer to two species of minke whale — the Antarctic minke whale (B. bonaerensis) and the dwarf minke whale (B. acutorostrata) — however, in the context of this review both are referred to as minke whales. 2. Common dolphins: three species of common dolphins have been identified — the short-beaked common dolphin (D. delphis), the long-beaked common dolphin (D. capensis) and the Arabian common dolphin (D. tropicalis) — however, in the context of this review all are referred to as common dolphins due to the overlap in distribution of D. delphis and D. capensis. Source: Based on Ridgeway & Harrison 1985, Rice 1998, Mann et al. 2000, Perrin et al. 2002, Reid et al. 2003b, IUCN 2004, Kaschner 2004.

Baleen whale migrations have generally been regarded as a response to the need to feed in colder waters and reproduce in warmer waters. Explanations for such long-range migrations have included (i) direct benefits to the calf, for example, increase in survival in calm, warm waters, (ii) relict from times when continents were closer together, (iii) the possible ability of some species to supplement their food supply with plankton encountered on migration or on calving grounds, (iv) reducing the risk of killer whale predation of new born calves in low latitudes and (v) species with a large body size (and lower mass specific metabolic rates) are able to make the long migrations that allow them to take advantage of warmer, and predator-free, waters (Bannister 2002, Stern 2002). The movements of odontocetes (toothed whales) vary more in scale depending on geographic range and species. For example, some sperm whales (Physeter macrocephalus) undertake long seasonal migrations similar to those of baleen whales, between high-latitude feeding grounds and warmer water breeding areas, although this is probably quite unusual in odontocetes (Whitehead 2002). Large seasonal movements often occur in oceanic odontocetes, for example, Stenella species and common dolphins (Delphinus delphis). Coastal bottlenose dolphins (Tursiops truncatus) exhibit

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a full spectrum of movements, including seasonal migrations, year-round home ranges, periodic residency and occasional long-range movements (Wells & Scott 2002). Bottlenose dolphins living at the high-latitude or cold-water extremes of the species’ range may migrate seasonally, for example, along the Atlantic coast of the U.S. (Wells & Scott 2002). North-south and inshoreoffshore seasonal movements have been observed in several odontocete species, including harbour porpoise (Phocoena phocoena) (Northridge et al. 1995, Anderson et al. 2001, Bjørge & Tolley 2002). Dispersal and migration is common in several pinniped species. Sea lion species, such as the California sea lion (Zalophus californianus), tend to live in warmer areas where food resources are more constant and there is less dispersal from breeding sites. However, Phocidae species (true seals) that live in higher latitudes, which are more dependent on ice cover and/or seasonally changing prey, tend to have a wider dispersal. For example, northern and southern elephant seals (Mirounga angustirostris and M. leonina) spend between 8 and 10 months at sea each year, with long-distance migrations from breeding and moulting sites to feeding areas (Forcada 2002). Polar bears undertake seasonal migrations, and these long-range movements are generally related to ice cover and seal distribution (Forcada 2002). Sirenians, such as manatees (Trichechus manatus), also embark on seasonal movements. For example in Florida, where water temperature is a major determinant factor (Reynolds & Powell 2002). Migration and the range of marine mammal species have evolved within constantly changing environmental conditions. Species have adapted to historic changes in climate. However, many of these changes, such as the retreat of the polar front in the Pleistocene, occurred at a rate that allowed species to adapt. Although marine mammals are capable of adapting to environmental changes, it is unclear if they will be able to adapt at the rate of climate change predicted in the near future (Stern 2002). Wild species have three basic possible responses to climate change: (i) change geographical distribution to track environmental changes; (ii) remain in the same place but change to match the new environment, through either plastic response, such as shifts in phenology (for example timing of growth, breeding, etc.) or genetic response, such as an increase in the proportion of heat tolerant individuals; or (iii) extinction (IPCC 2001a).

Climate change Future changes in the global climate are difficult to predict. The climate system is made up of a number of components: the atmosphere, oceans, land surface, cryosphere (ice areas) and biosphere (including human influences). Each of these systems is the result of a large array of drivers and climate is a result of complex interactions between each of the components. The only way to make quantitative predictions about future changes in climate is through the use of Global Climate Models (GCM) which simulate future climates given an emissions scenario and a mathematical representation of climate processes. Currently, there are hundreds of climate scenarios described in the literature. These scenarios, which cover both global and regional areas, have been developed for a variety of purposes and consider a large range of possible emission levels and other factors. Currently, the most extensively used scenarios, and those referred to in this review, are compiled by the Intergovernmental Panel on Climate Change (IPCC) in its Third Assessment Report (IPCC 2001b). The observed and predicted effects of global climate change vary between areas. Examples from the U.K. and surrounding waters have been included as an indication of these changes, as there is a long-time series for climate data and there have been intense efforts to predict future changes. The predicted changes for the U.K. are based on the U.K. Climate Impacts Program (UKCIP) scenarios, which provide the most comprehensive assessment of climate change impacts in the U.K. (Hulme et al. 2002).

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Changes in temperature Globally the average surface temperature (the average of near surface air temperature over land and sea surface temperature) has increased over the twentieth century by 0.6 ± 0.2˚C, with an increase of 0.4–0.7˚C in marine air temperature and a 0.4–0.8˚C increase in sea-surface temperature since the late-nineteenth century (IPCC 2001b). The global ocean heat content has increased significantly since the late 1950s, with more than half of the increase occurring in the upper 300 m of the ocean, this is equivalent to a rate of temperature increase in this layer of about 0.04˚C/decade (IPCC 2001b). The globally averaged surface (sea and land) temperature is projected to increase by 1.4–5.8˚C over the period 1990–2100 (IPCC 2001b). Projections indicate that the warming would vary by region (IPCC 2001a). In most areas of the North Atlantic during 2003, temperature in the upper water layers remained higher than the long-term average, with new records set in several regions (ICES 2004). Over the northern North Sea, average air temperatures have risen by 0.8˚C since 1960. Since 1995, winter sea temperatures in Scottish coastal waters have been warming faster than summer ones, resulting in a smaller annual range each year. Winter seabed temperatures at fishing grounds in the North Sea show a long-term warming trend since the 1970s. Over the last 30 yr, Scottish offshore waters have also warmed by between 1 and 1.5˚C. In oceanic waters at the edge of the U.K.’s continental shelf there has been a steady rise in temperature over the past 100 yr (FRS 1998, 2003). There has been an overall warming of U.K. coastal waters, with an increase in annually averaged temperature of about 0.6˚C over the past 70–100 years, with a substantial increase over the last 20 yr (Hulme et al. 2002). Climate change scenarios for the U.K. predict that the annual temperature across the U.K. may rise by between 2 and 3.5˚C by the 2080s. The temperature of U.K. coastal waters will also increase, although not as rapidly as over land. Offshore waters in the English Channel may warm in summer by between 2 and 4˚C over the same period (Hulme et al. 2002).

Changes in sea levels Tide gauge data show that global average sea level rose between 0.1 and 0.2 m during the twentieth century (IPCC 2001b). Global mean sea level is projected to rise by 0.09–0.88 m between 1990 and 2100. The geographical distribution of sea-level changes results from interactions between factors such as the geographical variation in thermal expansion, and changes in salinity, winds and ocean circulation. Therefore the range of regional variation is substantial compared with the global average sea level rise (IPCC 2001b). Climate change scenarios for the U.K. predict that by the 2080s sea levels may be between 2 cm below and 58 cm above the current level in western Scotland and between 26 and 86 cm above the current level in southeast England, depending on the climate change scenario and effects of land movements. Extreme sea levels, occurring through combinations of high tides, sea-level rise and changes in winds, are also predicted to become more frequent at many U.K. coastal locations (Hulme et al. 2002). A rise in sea level is likely to affect most coastal habitats, although the extent will vary with location and type of coastal habitat. Many coastal areas are already experiencing increased levels of sea flooding, accelerated coastal erosion and seawater intrusion into freshwater sources and these processes will increase with climate change and rises in sea levels (IPCC 2001a). Low-latitude tropical and subtropical coastlines are highly susceptible to climate change impacts (IPCC 2001a).

Changes in ocean circulation In the Arctic, as temperature increases, more freshwater from melting snow and ice will be released into the North Atlantic, through the Fram Strait between northeastern Greenland and Svalbard. This 442

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could exert a strong influence on salinity in the North Atlantic, shift the Gulf Stream current, and even affect upwelling related to the Great Ocean Conveyor Belt current system (Tynan & DeMaster 1997, Marotzke 2000). Most models show a weakening of the ocean thermohaline circulation, which will lead to a reduction of heat transport into high latitudes of the Northern Hemisphere. The current projections using climate models do not exhibit a complete shutdown of the thermohaline circulation by 2100. Beyond 2100, the thermohaline circulation could completely, and possibly irreversibly, shut down in either hemisphere (IPCC 2001b). Climate change scenarios predict a weakening of the Gulf Stream during the twenty-first century, perhaps by as much as 25% by 2100, although a shutdown of the Gulf Stream is not predicted in any climate models (Hulme et al. 2002). Shifts in the locations of fronts and upwellings are also expected as the climate changes, but are difficult to predict.

Changes in sea-ice extent There has been a retreat of sea-ice extent in the Arctic spring and summer by about 10–15% since the 1950s. It is likely that there has been about a 40% decline in Arctic sea-ice thickness during the late summer to early autumn in recent decades and a slower decline in winter sea-ice thickness (IPCC 2001b). In the Northern Hemisphere snow cover and sea-ice extent are projected to decrease further (IPCC 2001b). Over the past 100–150 yr, observations show that there has probably been a reduction of about two weeks in the annual duration of lake and river ice in the mid to high latitudes of the Northern Hemisphere (IPCC 2001b). The sea-ice extent in Antarctica appears to be more stable, with no readily apparent relationship between decadal changes in Antarctic temperatures and sea-ice extent since 1973 (IPCC 2001b). However, the Antarctic Peninsula ice shelves have retreated over the last century, resulting in the collapse of the Prince Gustav and parts of the Larsen ice shelves in 1995 (Vaughan & Doake 1996, IPCC 2001b).

Changes in salinity Changes in salinity may occur as a result of increased evaporation with increased temperature and changes in ocean circulation. There may also be more localised changes in salinity as a result of changes in precipitation and associated river input and land run-off or the melting of ice sheets. In most areas of the North Atlantic during 2003, salinity in the upper layers remained higher than the long-term average, with new records set in several regions (ICES 2004). The salinity of Scottish oceanic waters has generally increased, with values approaching the highest recorded over the past 100 yr. This may indicate the arrival of warmer, more saline waters from further south in the Atlantic (FRS 1998). In southern North Sea fishing areas (e.g., German Bight), there is an apparent trend of decreasing salinity at the sea bed in winter, which may be linked to freshwater inputs from rivers around the coast (FRS 2003). Inshore waters off the northeast of Scotland have experienced a decrease in salinity in the past 5 yr (FRS 2003).

Changes in CO2 concentrations and pH The atmospheric concentration of carbon dioxide (CO2) has increased by 31% since 1750. The rate of increase over the past century is unprecedented during the past 20,000 yr, with the present atmospheric CO2 increase being caused by anthropogenic emissions of CO2 (IPCC 2001b). The oceans absorb CO2 from the atmosphere and in the past 200 yr the oceans have absorbed approximately half of the CO2 produced by fossil fuel burning and cement production (Royal Society 2005). The uptake of anthropogenic CO2 by the oceans will continue to increase with increasing atmospheric CO2 concentrations. However, warming will reduce the solubility of CO2 and increased 443

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temperatures will also increase vertical stratification (decreasing mixing between ocean layers), which will also reduce CO2 uptake by the oceans (IPCC 2001b, Royal Society 2005). Increasing atmospheric CO2 concentration has no significant fertilisation effect on marine biological productivity, but it decreases pH (IPCC 2001b). It is estimated that this uptake of CO2 has led to a reduction in the pH of surface waters by 0.1 units, which is the equivalent to a 30% increase in the concentration of hydrogen ions. Surface waters (