Root Feeders

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ROOT FEEDERS An Ecosystem Perspective

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ROOT FEEDERS An Ecosystem Perspective

Edited by

Scott N. Johnson

Philip J. Murray

SCRI, Invergowrie Dundee, DD2 5DA Scotland, UK

North Wyke Research Okehampton Devon EX20 1NU, UK

CABI is a trading name of CAB International CABI Head Office Nosworthy Way Wallingford Oxfordshire OX10 8DE UK Tel: + 44 (0)1491 832111 Fax: + 44 (0)1491 833508 E-mail: [email protected] Website: www.cabi.org

CABI North American Office 875 Massachusetts Avenue 7th Floor Cambridge, MA 02139 USA Tel: + 1 617 395 4056 Fax: + 1 617 354 6875 E-mail: [email protected]

© CAB International 2008. All rights reserved. No part of this publication may be reproduced in any form or by any means, electronically, mechanically, by photocopying, recording or otherwise, without the prior permission of the copyright owners. A catalogue record for this book is available from the British Library, London, UK. Library of Congress Cataloging-in-Publication Data Root feeders: an ecosystem perspective/edited by Scott N. Johnson and Philip J. Murray. p. cm. ISBN 978–1–84593–461–3 (alk. paper) 1. Insect nematodes–Ecology. 2. Roots (Botany)–Ecology. I. Johnson, Scott N. II. Murray, Philip J. III. Title. SB998.I57.R66 2008 632′.7--dc22 2008017801 ISBN-13: 978 1 84593 461 3 Typeset by SPi, Pondicherry, India. Printed and bound in the UK by Cromwell Press, Trowbridge.

Contents

Contributors

vii

Foreword

ix

Acknowledgements

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Introduction: Root Feeders – An Ecosystem Perspective S.N. Johnson and P.J. Murray

xiii

Part I: Techniques for Studying Root Feeders 1

Methods for Studying Root Herbivory L.A. Dawson and R.A. Byers

2

New Experimental Techniques for Studying Root Herbivores R.W. Mankin, S.N. Johnson, D.V. Grinev and P.J. Gregory

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20

Part II: Root Feeders in Context 3

Root Herbivory in Agricultural Ecosystems R.P. Blackshaw and B.R. Kerry

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4

Root Herbivory in Grassland Ecosystems T.R. Seastedt and P.J. Murray

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5

Root Herbivory in Forest Ecosystems M.D. Hunter

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Contents

6

Grape Phylloxera: An Overview K.S. Powell

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7

Using Biocontrol Against Root-feeding Pests, with Particular Reference to Sitona Root Weevils S.L. Goldson and P.J. Gerard

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8

Invasive Root-feeding Insects in Natural Forest Ecosystems of North America D.R. Coyle, W.J. Mattson and K.F. Raffa

134

Part III: Root Feeders in the Wider Ecosystem 9

Linking Aboveground and Belowground Herbivory S.N. Johnson, T.M. Bezemer and T.H. Jones

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10

Root Feeders in Heterogeneous Systems: Foraging Responses and Trophic Interactions G.N. Stevens, K.O. Spence and E.E. Lewis

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11

Climate Change Impacts on Root Herbivores J.T. Staley and S.N. Johnson

192

Species Index

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Subject Index

221

Contributors

T.M. Bezemer, NIOO-KNAW, Centre for Terrestrial Ecology, PO Box 40, 6666 ZG Heteren, The Netherlands & Laboratory of Nematology, Wageningen University and Research Centre, PO Box 8123, 6700 ES Wageningen, The Netherlands. E-mail: [email protected] R.P. Blackshaw, B426, Portland Square, Drake Circus, University of Plymouth, Plymouth, Devon PL4 8AA, UK. E-mail: [email protected] R.A. Byers, Formerly at Pennsylvania State University, Now: 205 Homestead Lane, Boalsburg, PA 16827, USA. E-mail: [email protected] D.R. Coyle, University of Wisconsin, Department of Entomology, 345 Russell Labs, 1630 Linden Drive, Madison, WI 53706, USA. E-mail: dcoyle@entomology. wisc.edu L.A. Dawson, The Macaulay Institute, Craigiebuckler, Aberdeen, AB15 8QH, UK. E-mail: [email protected] P.J. Gerard, AgResearch Ltd, Ruakura Research Centre, East Street, Private Bag 3123, Hamilton 3240, New Zealand. E-mail: [email protected] S.L. Goldson, AgResearch Ltd, Lincoln Research Centre, Springs Road and Gerald Street, Private Bag 4749, Christchurch 8140, New Zealand. E-mail: Stephen. [email protected] P.J. Gregory, SCRI, Invergowrie, Dundee, DD2 5DA, Scotland, UK. E-mail: Peter. [email protected] D.V. Grinev, SIMBIOS Centre, Level 5, Kydd Building, University of Abertay Dundee, Bell Street, Dundee DD1 1HG, UK. E-mail: [email protected] M.D. Hunter, University of Michigan, Department of Ecology and Evolutionary Biology, and School of Natural Resources and Environment, 1141 Kraus Natural vii

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Contributors

Science Building, 830 North University, Ann Arbor, MI 48109, USA. E-mail: [email protected] S.N. Johnson, SCRI, Invergowrie, Dundee, DD2 5DA, Scotland, UK. E-mail: [email protected] T.H. Jones, Cardiff School of Biosciences, Cardiff University, Cardiff CF10 3US, UK. E-mail: [email protected] B.R. Kerry, Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, UK. E-mail: [email protected] E.E. Lewis, Department of Nematology, University of California, Davis, One Shields Avenue, Davis, CA 95616, USA. E-mail: [email protected] R.W. Mankin, United States Department of Agriculture, ARS, CMAVE, 1700 SW 23rd Drive, Gainesville, FL 32608–1069, USA. E-mail: Richard.Mankin@ars. usda.gov W.J. Mattson, USDA Forest Service, Northern Research Station, Institute for Applied Ecosystem Studies, 5985 Highway K, Rhinelander, WI 54501-9128, USA. E-mail: [email protected] P.J. Murray, North Wyke Research, Okehampton, Devon EX20 1NU, UK. E-mail: [email protected] K.S. Powell, Department of Primary Industries, Biosciences Research Division, RMB 1145, Chiltern Valley Road, Rutherglen, Victoria 3685, Australia. E-mail: [email protected] K.F. Raffa, University of Wisconsin, Department of Entomology, 345 Russell Labs, 1630 Linden Drive, Madison, WI 53706, USA. E-mail: [email protected] T.R. Seastedt, Department of Ecology and Evolutionary Biology, Institute of Arctic and Alpine Research, University of Colorado, Boulder, CO 80309–0450, USA. E-mail: [email protected] K.O. Spence, Department of Nematology, University of California, Davis, One Shields Avenue, Davis, CA 95616, USA. E-mail: [email protected] J.T. Staley, Imperial College London, Silwood Park Campus, Buckhurst Road, Ascot, Berkshire, SL5 7PY, UK. E-mail: [email protected] G.N. Stevens, College of Natural Sciences and Mathematics, Ferrum College, Ferrum, VA, USA. E-mail: [email protected] D.H. Wall, NESB B244, Natural Resource Ecology Laboratory, Campus Mail 1499, Colorado State University, Fort Collins, CO 80523-1499, USA. E-mail: diana@nrel. colostate.edu

Foreword

Agriculturists and horticulturists have been concerned for a long time with the role of root feeders as pests of crops and forage plants, and with the economic losses that result from their activities. More recently, increased interest in the roles of root feeders in ecosystems has opened up this topic to a much wider range of researchers from diverse disciplines. Since the size of root systems often exceeds that of aerial parts of plants, it is perhaps surprising that belowground herbivores have received much less attention than aboveground herbivores, especially in the ecological literature. While there is now emerging a set of studies from different root-feeding organisms functioning in both natural and man-managed ecosystems, there has been little attempt to synthesize the knowledge resulting from this rich diversity of experience. Meeting this challenge was the impetus for a workshop at the University of Reading, UK, ‘Integrative approaches for the investigation of root herbivory in agricultural and natural systems’ held in September 2004. Contributors to the workshop offered a range of insights into the many facets of root herbivory, and it became obvious that such organisms were an integral part of many ecosystem processes. This book is based on presentations at the workshop, but also draws on the expertise of other contributors to produce an overview of root-feeding invertebrates. It aims to bring a range of viewpoints and approaches ‘under one roof’, covering everything from food web ecology to the potential impacts of climate change on root feeders.

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Foreword

We hope that this book will encourage others to delve deeper into this relatively unexplored topic, and to add to the understanding of the roles of belowground herbivores in the functioning of ecosystems. Peter J. Gregory Chief Executive and Institute Director Scottish Crop Research Institute Dundee, Scotland, UK Diana H. Wall Senior Research Scientist and Former Director Natural Resource Ecology Laboratory Professor, Department of Biology Colorado State University, USA

Acknowledgements

First of all, we would like to extend our warmest thanks to all of the contributors to this book, who have approached this project with incredible enthusiasm and a wealth of ideas. At SCRI, we would like to sincerely thank Philip Smith for proofreading all the chapters contained within this volume and to Ian Pitkethly for assisting with many of the graphics. Without their skillful assistance, our task would have been considerably more difficult. We would also like to extend our thanks to the Biotechnology and Biological Sciences Research Council (BBSRC) of the UK for funding the workshop (grant reference ISIS 1310) that gave the impetus to the writing of this volume, and all those who originally participated in the workshop. Finally, we would like to thank all of the staff at CABI involved in the production of this book for their continued assistance and patience. Scott Johnson acknowledges the support of the Scottish Government Rural and Environment Research and Analysis Directorate (RERAD), which provides grant in aid to SCRI. Phil Murray acknowledges the support of BBSRC, which provides support to North Wyke Research.

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Introduction: Root Feeders – An Ecosystem Perspective S.N. JOHNSON1 AND P.J. MURRAY2 1

Scottish Crop Research Institute, Dundee, UK; 2North Wyke Research, Okehampton, Devon, UK

Research on plants and their herbivores has traditionally been dominated by studies looking at interactions occurring aboveground, ranging from large mammals to the smallest invertebrates. The mechanisms and processes underpinning herbivory have been explored in almost all terrestrial ecosystems, ranging from agricultural monocultures to diverse forests and grasslands. Aboveground herbivory has been studied either ‘positively’ in terms of maximizing production of meat for human consumption, or ‘negatively’ in terms of controlling pest populations that reduce plant yields. By comparison, belowground herbivory by both vertebrates (e.g. rodents) and invertebrates (e.g. nematodes and insects) has been less well studied (Andersen, 1987; Brown and Gange, 1990; Hunter, 2001). Given that there is ample evidence from diverse ecosystems that >50% of net primary productivity is frequently allocated to the roots, which can approach 90% in some cases (Coleman, 1976), this seems to be paradoxical at first sight. The truth is that root feeders are, by their very nature, soil dwelling and therefore less visible, which has perhaps given rise to an ‘out of sight, out of mind’ attitude among researchers (Hunter, 2001). However, there is little doubt that root herbivores can be of considerable importance within an ecosystem. For example, root-xylem-feeding cicadas in eastern deciduous forests of North America have the highest collective biomass of any terrestrial animal when considered in terms of biomass per unit area (Karban, 1980). Because root feeders are less visible, their presence is often only obvious when they have significant impacts on plant growth and development, particularly in agricultural systems. Indeed, it is in agricultural systems that belowground herbivores have received the most detailed attention to date (see Blackshaw and Kerry, Chapter 3), with the economic consequences of root herbivory driving the research agenda towards those root feeders classified as pests. The emphasis of research has generally been orientated around direct control of root feeders (usually chemical pesticides), but lately, biological xiii

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control has been considered (Rasmann et al., 2005; Turlings and Ton, 2006), fuelling interest in trophic interactions occurring belowground (see Stevens et al., Chapter 10). Root feeders are not always the ‘enemy’, however, and there is now considerable interest in exploiting them as biological control agents of invasive plant species (Blossey and Hunt-Joshi, 2003). Blossey and Hunt-Joshi (2003) concluded that 54% of released root-feeding insects contributed to the suppression of invasive plant species, whereas only 34% of aboveground insect herbivores did so. However, other research shows that root feeders can actually make invasive plants more competitive (Callaway et al., 1999; Thelen et al., 2005), which further highlights the need to understand the fundamental mechanisms underpinning root–herbivore interactions. In mixed plant communities, root herbivores are often abundant but their effects are less obvious and of lower perceived economic importance. However, there is an increasing body of evidence that root feeding fundamentally affects many other, seemingly unconnected, ecosystem functions or services (Bardgett, 2005). In particular, root feeders can drive community dynamics of plants (De Deyn et al., 2003), soil microorganisms (Grayston et al., 2001; Treonis et al., 2005) and populations of aboveground organisms (Wardle et al., 2004), including other herbivores (see Johnson et al., Chapter 9). The realization that root feeders play such a key role in many ecosystem processes has undoubtedly reinvigorated interest in root herbivory research, and has shifted the emphasis from a purely applied viewpoint to one that incorporates a more holistic ecosystem perspective. In this book, we have invited 23 internationally renowned researchers working in the field of root herbivory to participate in this focused edited volume. Their work brings together current knowledge relating to belowground herbivory in 11 chapters, across a spectrum of areas and predicts the future challenges and directions for root herbivory research. We concentrate on root-feeding invertebrates (nematodes, and particularly insects) as this is the most widespread type of root herbivore and the focus of most contemporary research in root herbivory. The opening two chapters address the problems of visualizing the organisms in the soil and describe both conventional approaches and more modern techniques. First, Dawson and Byers (Chapter 1) review the major traditional techniques for investigating the impacts of root herbivory, including slant boards, cone containers, growth bags, rhizotrons and other visual techniques used in the laboratory and glasshouse, in addition to established field methods. These techniques can be classified as either destructive, where a single set of observations are made at the termination of the experiment, or non-destructive, which allow sequential observations or measurements to be made during the experiment. We summarize the salient findings of studies that use these techniques to illustrate the parameters and responses that can be quantified. Second, Mankin et al. (Chapter 2) focus on recent developments and potential of non-invasive methods for studying root herbivores in situ, both in the field (acoustic detection) and the laboratory (X-ray tomography). Such techniques are constantly under development and, like all techniques,

Introduction

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have limitations. They do, however, provide real potential for unravelling some of the more subtle interactions between roots and their herbivores. The following three chapters review the role of root herbivores in three important ecosystems: agriculture, grasslands and forestry. To explore aspects of root herbivory in agricultural systems (Chapter 3) in greater detail, Blackshaw and Kerry use two examples, the leatherjacket Tipula paludosa Meigen (Diptera: Tipulidae) and the potato cyst nematode Globodera pallida (Stone) (Tylenchida: Heteroderidae), and provide an overview of the biology, crop damage and management of these destructive pests. Seastedt and Murray provide a brief overview of the root-feeding herbivore groups that they consider to be most influential in grassland systems (Chapter 4). They discuss the impacts of these organisms on the productivity of grasslands and suggest several approaches to assessing both the direct and indirect effects of root feeders on grasslands. They also make some predictions as to how current trends in environmental characteristics (i.e. changes in atmospheric chemistry and plant composition) might affect our assessment of plant–soil herbivore interactions. Hunter (Chapter 5) provides a comprehensive overview of our current understanding of root herbivory in forest ecosystems, which is perhaps the least documented of the three ecosystems we cover. These overviews are followed by three in-depth considerations of specific examples related to root herbivory. First, Powell (Chapter 6) provides a review of grape phylloxera, Daktulosphaira vitifoliae (Fitch) (Hemiptera: Sternorrhyncha), and its impact on viticulture and current thinking behind control and management practices. Because grape phylloxera is such an important pest of a high-value crop, management and control strategies against this pest are particularly well developed, and this chapter perhaps provides the most detailed example of root herbivore management. Second, Goldson and Gerard (Chapter 7) discuss the introductions of two biotypes of the parasitic wasp Microctonus aethiopoides Loan (Hymenoptera: Braconidae) to control two weevils, the lucerne weevil Sitona discoideus Gyllenhal (Coleoptera: Curculionidae) and the clover root weevil S. lepidus Gyllenhal (Coleoptera: Curculionidae) in New Zealand. This is presented as a case study with which to explore the potential of biocontrol agents against root herbivores. While it is the root-feeding life stages (the larvae) that actually cause the damage to plants, in this case the biocontrol agent is targeted at the aboveground life stages (the adults), illustrating the need to consider aboveground aspects of the lifecycle when controlling the root feeder. Third, Coyle et al. (Chapter 8) focus on invasive root-feeding weevils in natural forest systems of North America and discuss how this group of root herbivores has displaced a whole range of native fauna. In compiling this book, we aimed to review our existing knowledge about root feeders, and also illustrate that root herbivores are an influential component of the wider ecosystem, connected by complex interactions with other organisms. The final three chapters therefore consider root feeders in the wider ecological context. Increasingly, the linkages between belowground and aboveground systems are the focus of much attention in the ecological literature (Wardle et al., 2004). Johnson et al. (Chapter 9) review existing

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examples of plant-mediated interactions between aboveground and belowground insect herbivores and explore the mechanisms underpinning such interactions, with particular emphasis on how root-feeding insects change host plants in a manner that potentially affects aboveground communities. They raise the issue of how trophic complexity is increasingly becoming central to our understanding of aboveground–belowground interactions, and attempt to identify future research questions. This is followed by a review by Stevens et al. (Chapter 10) focusing on interactions among plants, root feeders and nematodes. This is principally at the sub-metre scale, which is the approximate scale of heterogeneity that is perceived by a larval insect root feeder, plant root or nematode. Finally, as there is a general consensus among scientists that the earth’s climate is currently changing at a more rapid pace than at any point in its history, Staley and Johnson (Chapter 11) discuss the direct and indirect effects of climate change on root-feeding invertebrates. They comment on how there is good evidence for how direct effects of climate change (e.g. drought) will affect root herbivores, but very little information that explicitly links the indirect (i.e. plant-mediated) impacts of climate change and root herbivores, despite evidence that roots are frequently the most affected part of the plant. They also speculate on how interactions between foliar and root-feeding herbivores may be altered in a changing climate. The ethos of this book, therefore, is to bring together both the agricultural and ecological perspectives of root herbivory in order to synthesize what information is currently available to researchers and identify the challenges that lie ahead. With this approach we aim to stimulate a better understanding of the unseen herbivores that live beneath us.

References Andersen, D.C. (1987) Belowground herbivory in natural communities – a review emphasizing fossorial animals. Quarterly Review of Biology 62, 261–286. Bardgett, R.D. (2005) The Biology of Soil: A Community and Ecosystem Approach, 1st edn. Oxford University Press, Oxford. Blossey, B. and Hunt-Joshi, T.R. (2003) Belowground herbivory by insects: influence on plants and aboveground herbivores. Annual Review of Entomology 48, 521–547. Brown, V.K. and Gange, A.C. (1990) Insect herbivory below ground. Advances in Ecological Research 20, 1–58. Callaway, R.M., DeLuca, T.H. and Belliveau, W.M. (1999) Biological control herbivores may increase competitive ability

of the noxious weed Centaurea maculosa. Ecology 80, 1196–1201. Coleman, D.C. (1976) A review of root production processes and their influence on soil biota in terrestrial ecosystems. In: Anderson, J.M. and Macfadyen, A. (eds) The Role of Terrestrial and Aquatic Organisms in Decomposition Processes. Blackwell, Oxford, pp. 417–434. De Deyn, G.B., Raaijmakers, C.E., Zoomer, H.R., Berg, M.P., de Ruiter, P.C., Verhoef, H.A., Bezemer, T.M. and van der Putten, W.H. (2003) Soil invertebrate fauna enhances grassland succession and diversity. Nature 422, 711–713. Grayston, S.J., Dawson, L.A., Treonis, A.M., Murray, P.J., Ross, J., Reid, E.J. and MacDougall, R. (2001) Impact of root

Introduction herbivory by insect larvae on soil microbial communities. European Journal of Soil Biology 37, 277–280. Hunter, M.D. (2001) Out of sight, out of mind: the impacts of root-feeding insects in natural and managed systems. Agricultural and Forest Entomology 3, 3–9. Karban, R. (1980) Periodical cicada nymphs impose periodical oak tree wood accumulation. Nature 287, 326–327. Rasmann, S., Köllner, T.G., Degenhardt, J., Hiltpold, I., Toepfer, S., Kuhlmann, U., Gershenzen, J. and Turlings, T.C.J. (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434, 732–737. Thelen, G.C., Vivanco, J.M., Newingham, B., Good, W., Bais, H.P., Landres, P., Caesar, A. and Callaway, R.M. (2005) Insect herbivory

xvii stimulates allelopathic exudation by an invasive plant and the suppression of natives. Ecology Letters 8, 209–217. Treonis, A.M., Grayston, S.J., Murray, P.J. and Dawson, L.A. (2005) Effects of root feeding, cranefly larvae on soil microorganisms and the composition of rhizosphere solutions collected from grassland plants. Applied Soil Ecology 28, 203–215. Turlings, T.C.J. and Ton, J. (2006) Exploiting scents of distress: the prospect of manipulating herbivore-induced plant odours to enhance the control of agricultural pests. Current Opinion in Plant Biology 9, 421–427. Wardle, D.A., Bardgett, R.D., Klironomos, J.N., Setälä, H., van der Putten, W.H. and Wall, D.H. (2004) Ecological linkages between aboveground and belowground biota. Science 304, 1629–1633.

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I

Techniques for Studying Root Feeders

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1

Methods for Studying Root Herbivory L.A. DAWSON1 AND R.A. BYERS2 1

The Macaulay Institute, Aberdeen, UK; 2Pennsylvania State University, USA

1.1. Introduction This chapter reviews the major traditional techniques for investigating the impacts of root herbivory, including slant boards, cone containers, growth bags, rhizotrons and other visual techniques used in the laboratory and glasshouse, in addition to established field methods. These techniques can be classified as either destructive, where a single set of observations are made at the termination of the experiment, or non-destructive, which allow sequential observations or measurements to be made during the experiment. We summarize the salient findings of studies that use these techniques to illustrate the parameters and responses that can be quantified.

1.2. Destructive Laboratory and Glasshouse Techniques 1.2.1. Laboratory apparatus Several techniques and container types have been used to rear root-feeding insects in the laboratory. For example, Dobrovsky (1954) studied wireworms (Elateridae) in the laboratory by rearing larvae in test tubes. Test tubes were filled with moist soil and a single newly hatched larva was introduced into each tube. Byers (1995) reared Sitona hispidulus (Fabricius) (Coleoptera: Curculionidae) using legumes growing in cone containers in a growth chamber. Legume species studied were white clover (Trifolium repens L.), red clover (T. pratense L.) and lucerne (Medicago sativa L.). Eight factors were tested for their effect on insect rearing. The four most important factors were as follows: egg infestation rate, egg age, sterilization of egg surfaces and the peat– vermiculite mixture as plant growth medium. Legume species, plant age at the time of infestation, watering schedules (two, three or seven times per ©CAB International 2008. Root Feeders: An Ecosystem Perspective (eds Johnson and Murray)

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week) and number of holes for placing larvae in the soil had no impact on larval survival. Survival was improved using eggs rather than newly hatched larvae to infect plants. Taproot injury increased with increasing number of eggs, but not with the number of larvae per plant. There was a 30–50% recovery of male and female beetles compared to around 20% survival with other published rearing methods. In addition to rearing root herbivores, researchers have developed a range of laboratory apparatus for manipulative experiments involving root herbivores (Fig. 1.1). For example, an experiment using micro-lysimeters was carried out by Murray et al. (2002) to investigate root nodule herbivory by early-instar larvae of the clover root weevil, S. lepidus (Gyllenhal) (Coleoptera:

(A)

(B)

(C)

Fig. 1.1. Apparatus used for studying insect root herbivores. (A) Sitona hispidulus

(Fabricius) feeding on roots of lucerne Medicago sativa L. seedlings on a nutrient slant board technique in a growth chamber. (B) Microcosms that allowed for the collection of rhizosphere solutions (containing rhizodeposits and soluble larval wastes) for chemical characterization, while allowing root observations to be made. (C) Camera images (Bartz) of mini-rhizotron tube with (upper) and without (lower) regular application of insecticide (Dursban) on unimproved pasture. Note the ability with such methods to also observe grazers such as collembolans. White bar = 10 mm.

Methods for Studying Root Herbivory

5

Curculionidae), and its effect on assimilation of carbon (C) by plants of white clover. Each micro-lysimeter was constructed from the barrel of a 50 ml syringe with non-absorbent cotton wool packed at the base and filled with 50 cm3 of sterilized sand. The white clover plants were grown in individual growth chambers and the net C assimilation by each plant was estimated by monitoring CO2 flux in the chambers. White clover plants which had been infested with larvae had a significantly (P < 0.01) reduced biomass when compared with the control plants and tended to have a smaller root/shoot ratio (0.68 versus 0.78). The number of nodules on the clover roots was significantly (P < 0.05) reduced by the weevil infestation. Significant treatment differences in net C accumulation were evident only towards the end of the study period with the control plants showing a significant (P < 0.05) net gain of C from day 19 onwards. There are several examples of ‘soil olfactometers’ being used to investigate specific aspects of root herbivore ecology in glasshouse environments and controlled environment facilities. These have included studies of root herbivore interactions with natural enemies (Boff et al., 2001; Van Tol et al., 2001; Rasmann et al., 2005; Rasmann and Turlings, 2007) and host plant location behaviour (Bernklau and Bjostad, 1998; Johnson et al., 2004; Johnson and Gregory, 2006). In particular, Johnson et al. (2004) used ‘Y’-shaped ‘soil olfactometers’ to investigate host plant recognition by the clover root weevil, S. lepidus. The olfactometer was similar in design to that of Boff et al. (2001), in that it was composed of sections of soil-filled tubes that could be destructively sampled to ascertain the final location of S. lepidus larvae in relation to different plant species growing at opposing ends of the ‘Y-shaped’ olfactomer (see Johnson et al., 2004 for full details). They reported how newly born (neonatal) S. lepidus larvae could detect the presence of their preferred host plant (white clover, T. repens) from distances of either 25 or 60 mm from the roots. Moreover, S. lepidus larvae could distinguish and preferentially move towards white clover roots over roots of a non-host plant such as perennial ryegrass (Lolium perenne L.), and less suitable clover species such as subterranean clover (T. subterraneum L.) and strawberry clover (T. fragiferum L.) (Johnson et al., 2004).

1.2.2. Pot-based experiments in controlled environments Gange et al. (1991) studied the effect of root and hypocotyl herbivory on mortality of germinating seeds of the common vetch (Vicia sativa L.) in a pot trial under controlled conditions. They studied root-feeding chafers, Phyllopertha horticola (L.) (Coleoptera: Scarabaeidae), and crane fly larvae (also known as leatherjackets), Tipula paludosa (Meigen) (Diptera: Tipulidae), which were restricted by nylon mesh partitions to enable radicle and/or hypocotyl herbivory to occur. The effects of these two insects were very similar. In control situations, an average of 88% of the viable seed sown recruited successfully. Hypocotyl and radicle herbivory had similar effects on seedling mortality, with recruitment of viable seed sown being reduced to 52%. When both modes of attack occurred together, successful recruitment was only 34%.

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Feeding on both plant parts resulted in an average post-emergence mortality of 14% of the seed sown, but the effect on pre-emergence mortality was of greater importance, amounting to 41%. Dawson et al. (2004) conducted a study in a controlled environment facility, to examine the effect of larval feeding of T. paludosa on the soil microbial community, using pots under controlled environmental conditions. Bent grass (Agrostis capillaris L.) and white clover were grown in pots, in monoculture and as mixtures, containing soil from an upland grassland site in the UK. After plant establishment, larvae were added to half the pots at field density (480 larvae per m2). After 12 days, the pots were destructively harvested and the shoot biomass, root biomass and the soil microbial community (using plate counts and community-level physiological profiles; CLPP) were assessed. The presence of larvae significantly reduced shoot biomass in white clover growing as monoculture. In pots containing a mixture of bent grass and white clover, only the shoot biomass of the white clover was significantly reduced. In the single-species pots, the larvae significantly reduced the root biomass of both species. The soil microbial community structure changed in the presence of larvae, resulting in a significant tenfold increase in the numbers of Pseudomonas spp. in the soil. Canonical variate analysis of the CLPP data also showed that microbial communities from the soils with larvae present had a greater utilization of a number of sugars, amino acids and carboxylic acids. These changes might have arisen as a result of an increase in C exudation due to root severance or shoot herbivory, an increase in dead roots or due to larval decomposition or defecation.

1.2.3. Pot plant-based experiments in glasshouses Potted plants in a greenhouse are often used to study root herbivory and interactions between aboveground and belowground herbivory. Bezemer et al. (2003) grew cotton plants in large 7 l containers in a sand, peat and clay mixture (50:40:10). The four treatments studied were: (i) belowground herbivory; (ii) aboveground herbivory; (iii) both belowground and aboveground herbivory; and (iv) no herbivory. Individual plants in the root herbivory treatment were infested with late-instar wireworms, Agriotes lineatus (L.) (Coleoptera: Elateridae), that had been hand-collected from a pasture. Larval density was about 30 per m2. Plants in the aboveground herbivory treatment were infested with beet armyworms, Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae). Third-instar larvae were placed in clip cages coated with foam rubber to prevent plant damage. The outsides were covered with screen mesh. Larvae fed within the cage for 2 days were moved to a site on the same leaf. After 2 more days of feeding, the larvae were moved to a new leaf. Plants were exposed to this treatment for 5 weeks during which 20 cm2 was consumed on four leaves. Results showed that plants exposed to root herbivory alone had significantly lower root biomass than undamaged plants. A similar trend occurred for root and foliar herbivory (P = 0.059). However, neither root nor foliar herbivory influenced plant height, leaf numbers, stem, leaf or shoot biomass.

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Richmond et al. (2003) also used plastic pots in a glasshouse to study the effect of the root herbivore Japanese beetle, Popillia japonica (Newman) (Coleoptera: Scarabaeidae), and fungal endophytes on competition between turfgrass and dandelion, Taraxacum officinale (Webber). Plants were germinated in Petri dishes and seedlings of perennial rye grass and tall fescue (Festuca arundinacea Schreb.) were transplanted into soil using endophyte-infected and uninfected grass plants and dandelion. The fungal endophytes were Neotyphodium lolii for ryegrass and N. coenophialum for tall fescue. Treatments were monocultures of dandelion and endophyte-infected and uninfected tall fescue and ryegrass. Monocultures of dandelion had two pots with insect larvae and two were insect-free. Grass monocultures had four pots: two pots containing endophyte-infected plants and two uninfected. Of the two pots containing either endophyte-infected or uninfected grasses, one pot received insect larvae and the other remained insect-free. There were also treatments of mixtures of plant species using 50:50 mixtures of dandelion and grass. A single replicate consisted of eight pots: four containing dandelion and endophyteinfected grass and four with dandelion and uninfected grass. Two of the four pots received insect larvae and the other two remained insect-free. Three fieldcollected third-instar beetle larvae per pot were added to insect-designated treatments. After 2 months, plant shoots and roots were separated and evaluated with all larvae being recovered from the soil at the same time. All plant and insect materials were dried at 80°C for 48 h before measuring biomass. Results showed that herbivory by Japanese beetle larvae and endophyte infection reduced tiller production of perennial ryegrass and tall fescue in monocultures. Japanese beetle larvae displayed poor survival on dandelion and had no effect on dandelion leaves or belowground biomass. In plant mixtures, Japanese beetle larvae reduced tiller numbers and aboveground and belowground biomass of grasses, which benefited the dandelion through an increased leaf and belowground biomass. Japanese beetle herbivory had no effect on the performance of endophyte-infected or uninfected grasses. Stevens and Jones (2006), concerned with the lack of information relating to the role of herbivory in modifying plant resource interactions, conducted a glasshouse study in which nutrient heterogeneity and root herbivory (using Scarabaeidae grubs) were both manipulated. They used differences in foraging among plant species to predict the influence of root herbivores on these species in competition. They also tracked the influence of neighbourhood composition, heterogeneity and herbivory on whole-pot plant biomass. They found that when Scarabaeidae herbivores were added to the mixed-species neighbourhoods, Eupatorium compositifolium (Walter), the most precise plant forager, was the only plant species to display a reduction in shoot biomass. Neighbourhood composition had the greatest influence on whole-pot biomass, followed by nutrient heterogeneity; root herbivory had the smallest influence. These results suggest that root herbivory is a potential cost of morphological foraging in roots. Root herbivores reduced standing biomass and influenced the relative growth of species in mixed communities, but their effect was not strong enough at the density examined to overwhelm the bottom-up effects of resource distribution.

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The indirect effects of soil heterogeneity on the foraging behaviour of root herbivores were investigated by Stevens et al. (2007). They used sand-filled glasshouse pots to assess root herbivore foraging behaviour and potential interactions between patch quality, herbivore foraging and plant biomass production. Individual pots were divided into four quarters: one fertilized and three unfertilized (two of which were planted with tree seedlings). The two treatments used to create fertilized quarters were high-organic manure fertilizer and slow-release mineral fertilizer. Seedlings of red maple, Acer rubrum L., and Virginia pine, Pinus virginiana L., were used to create two single-species and one mixed-species treatments. Root-feeding beetle larvae were added to the pots and allowed to forage freely for 8 weeks. At the destructive harvest, results showed that root herbivores in the organic-fertilized pots were strongly attracted to fertilized quarters despite their relatively low root biomass. In the mineral-fertilized pots, larvae were most abundant in the planted quarters, which is also where most of the plant roots occurred. Whole-pot plant yield was significantly reduced by larvae; this effect was stronger in the mineralfertilized pots than in the organic-fertilized pots. While one of the plant species appeared more sensitive to herbivory, root herbivores had a greater influence on yield in mixed-species pots than in single-species pots. These results suggest that patch quality influences on herbivore foraging may indirectly alter yield and plant community composition.

1.2.4. Grow bags in protected environments A number of root herbivores flourish in protected environments such as plastic tunnels, where horticultural crops are often grown with plastic or mulch coverings around the base of the plant. The resulting warm and moist soil conditions are ideal for such pests, so little wonder that applied researchers have begun to conduct experiments in such conditions. For instance, control of black vine weevil, Otiorhynchus sulcatus (F.) (Coleoptera: Curculionidae), was examined using grow bags inoculated with nematodes (Lola-Luz et al., 2005). Strawberries were grown in commercial grow bags naturally infested with black vine weevil. Two nematode isolates used were Heterorhabditis medidis (UK211) and H. downsei (K122), both previously laboratory-cultured. Grow bags were inoculated with nematodes on one, two or three occasions. Nine days after infestation, nine blocks of each treatment were destructively harvested. Nematodes significantly increased O. sulcatus mortality, ranging from 51% to 94%.

1.3. Non-destructive Laboratory and Glasshouse Techniques 1.3.1. Slant boards Baker and Byers (1977) reared S. hispidulus (Fabricius) (Coleoptera: Curculionidae) on lucerne (M. sativa L.) seedlings in the growth chamber using

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a nutrient slant board technique, modified from the method described by Kendall and Leath (1974). The slant board culture unit was a plastic cafeteria tray with a surface of 31 × 41 cm and sides 2 cm tall with the long axis of the tray held in wire racks to a near vertical position. The portion of the tray that supported the plant roots was covered with a single layer of 100% polyester cloth. A second layer of polyester cloth covered the roots. About 3 l of vermiculite was enclosed in a polyester bag and placed on top of the second cloth. Sheet aluminium was fitted over the sides of the tray to cover the root growth area and held in place with paper binder clips. Trays were assembled in a horizontal position while the plants were placed on the cloths and nutrient solutions were used to soak the bags of vermiculite. Thereafter, the trays were held at an angle of 50° in galvanized wire racks of 80 × 40 × 26 cm height (seven trays per rack) and irrigated twice daily. Eggs from field-collected adults were used to infest the plants. Eggs were surface-sterilized by immersion for 20 min in 10% formaldehyde and rinsed in distilled water. Plants were infested by placing eggs near a root nodule, the feeding site of firstinstar larvae. After larval development was completed, the pupae were placed in cans containing sterilized moist sand and held at room temperature. A tiller of lucerne was placed in the can as food for emerging adults. Adults were pooled and held for 6 weeks on lucerne. After a preoviposition period of 6 weeks at 6°C, viable eggs and larvae were obtained. To investigate feeding preference of the adult clover root weevil S. lepidus on three red clover (T. pratense L.) lines, selected for high, medium or low levels of the isoflavone formononetin in foliage, Gerard et al. (2005) used a no-choice slant board experiment. Weevil larval weights were greater for larvae feeding on white clover roots than for those feeding on roots of the red clovers. The effect of larval root herbivory on plant growth was similar for all four clovers. Following root herbivory, a large increase in root and shoot formononetin levels was observed in the high-formononetin selection of red clover, but little change in the low-formononetin selection in red clover. In a no-choice experiment with sexually mature female adult weevils feeding on foliage of the four clovers, all the red clovers had increased weevil mortality. Female weevils consuming the high-formononetin red clover laid fewer eggs than weevils feeding on white clover. The red clover diet caused a large accumulation of abdominal fat and/or oil in the weevils, whereas weevils feeding on white clover did not accumulate fat or oil. When sexually immature adult weevils were given a choice of foliage from all four clovers, white clover was eaten preferentially, and the low-formononetin red clover was preferred to the high-formononetin red clover. The results suggest that formononetin and associated metabolites in red clover may act as chemical defences against adult S. lepidus and that distribution in forage legumes can be manipulated by plant breeding to improve root health. Byers and Kendall (1982) used the slant board method to assess the feasibility of locating resistance to S. hispidulus larvae and the effects of root nodules on the growth and survival of larvae. No resistance to S. hispidulus was found in diverse genotypes of lucerne, red clover and white clover; however, three cultivars of birdsfoot trefoil (Lotus corniculatus L.), one cultivar of crownvetch

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(Coronilla varia L.) and one cultivar of bigflower vetch (V. grandiflora var. kitaibeliana W. Koch) were resistant to S. hispidulus larvae. Growth, but not survival, of insect larvae was less on red clover roots without nodules than on fully nodulated roots. Both growth and survival were less on lucerne roots without nodules than on roots with nodules. Murray and Clements (1992) modified the slant board system to estimate losses to white clover roots by feeding from Sitona weevils. Loss of up to 50% of root length was found. The effects of root feeding by larvae of S. hispidulus (Fabricius) on the rate of transfer of nitrogen between plants of white clover and perennial ryegrass were investigated using a nutrient slant board technique (Murray and Hatch, 1994). Clover plants, labelled with 15N, were grown adjacent to unlabelled ryegrass plants and were either infested with Sitona larvae or not infested. Ryegrass plants associated with the infested clover plants had a significantly higher dry matter yield and nitrogen content than the insect-free plants, after 33 days exposure to insect herbivory. It was concluded that root-feeding insects could play an important role in the cycling of nitrogen in grass/clover swards. Using a slant board system, the effect of leatherjacket larvae (T. paludosa) on two pasture species (white clover and perennial ryegrass) was investigated by Dawson et al. (2002). The larvae fed voraciously on the main root axes of white clover, causing a 15% reduction in primary axis root length. In contrast, there was no overall effect of grazing on root length of ryegrass. However, the proportion of the root system of ryegrass present as laterals was reduced. The plant nitrogen content of white clover was reduced by grazing, possibly due to leakage of nitrogen-containing compounds or selectivity of nitrogen-rich tissues by the grazing invertebrate. Larvae were larger when fed on white clover and their faeces had a higher concentration of bacteria compared with those fed on ryegrass.

1.3.2. Microcosms, mini-rhizotrons and transparent plant pouches Non-destructive methods for the assessment of indirect effects of root herbivory on the soil microbial community have been developed (e.g. Treonis et al., 2005). In this study, the impacts of root feeding by crane fly T. paludosa larvae on rhizosphere chemistry and soil microbial communities were investigated using microcosms that allowed the collection of rhizosphere solutions (containing rhizodeposits and soluble larval wastes) for chemical characterization. Solutions were collected from the rhizospheres of three grassland plants (bent grass, white clover and perennial ryegrass) in microcosms with and without crane fly larvae. The activity of larvae resulted in significantly reduced plant biomass and enhanced organic C input to the rhizosphere solutions collected from ryegrass and white clover. For bent grass, plant biomass and rhizosphere solution organic C was not affected significantly by larvae, but this may have been a consequence of a lower larval biomass in this experiment. Solutions collected from all three plants contained more ammonium (NH+4) when larvae were present, likely due to the deamination of larval wastes. The presence of

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larvae also increased the amount of carbohydrates in solutions from bent grass and ryegrass, but carbohydrates decreased in solutions from white clover. Rhizosphere solutions were applied to soil and changes in microbial communities were assessed. Bacterial and fungal biomass increased in soils receiving solutions from ryegrass with larvae, as indicated by the quantity of microbial phospholipid fatty acid (PLFA) biomarker lipids extracted. Fungal biomass was also higher in soils receiving solutions from larvae-treated bent grass. Fungal biomass decreased and some Gram-positive biomarker PLFAs were reduced in soils receiving rhizosphere solutions from larvae-treated white clover. Analysis of CLPP showed significantly lower sugar use for soils receiving solutions from white clover with larvae, which correlates with the measured reduction in carbohydrate content. Through the use of this modified microcosm system, results suggest that the activity of these root-feeding larvae leads to shifts in soil microbial communities that are linked to changes in rhizosphere chemistry. Mini-rhizotron systems have been used in the laboratory to study tree growth. Wiese et al. (2005) describe a two-dimensional mini-rhizotron made with plexiglass for use in a greenhouse. Such an approach, using smalldiameter tubes, can also be used for studying root herbivory in a laboratory situation, although care has to be taken to ensure that a suitable size and shape of container is used for the plant and herbivore of interest. In addition, drainage effects and temperature and moisture differentials around the tube should be minimized. To account for such artefacts, mini-rhizotron tubes are often inserted at an angle to the soil surface, although consideration of root architecture is also important with choice of angle. Growth pouches were used by Quinn and Hall (1992) to study herbivory of legume root nodules and compensatory response in root growth. Plants were grown in clear plastic pouches and subjected to 23% denodulation by S. hispidulus larvae and 50% nodule pruning. Additional plants were untreated. Results showed that nodule herbivory and nodule pruning caused an overcompensatory response in a number of nodules.

1.4. Destructive Field Techniques Masters (2004) pointed out that there are two approaches for testing the implications of root herbivory for ecosystem structure and function under field conditions: adding or eliminating root feeders from the system and recording the response.

1.4.1. Container-based approaches using root feeder additions Examples of adding root feeders often involve infesting sunken containers in the field with root herbivores. Some containers used are clay or plastic pots or field tiles. For example, Bryson (1929) set two unglazed field tiles, 6 in. in diameter and 1 ft in length, end to end in a hole 22 in. deep. A smooth

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flat rock at the bottom of the lower tile prevented root herbivores from escaping. Field soil was sifted to remove any arthropods and placed in the tiles. Wheat (Triticum aestivum L.) and oats (Avena sativa L.) were planted as seeds in the tiles and later infested with 25 wireworms (Coleoptera: Elateridae) collected from the field and sorted to size. Wire screen in the shape of a cone was placed over the top of the tiles. The contents of the tiles were later destructively sampled an inch at a time and the location of the surviving adults was noted. Two hundred larvae out of 525 survived to the adult stage. This method offers opportunity to study feeding habits of the larvae. Poveda et al. (2003) used 10 l pots filled with soil taken from a 10-yearold fallow field to study the effects of wireworms (Elateridae: Agriotes sp.) on growth of mustard (Sinapis arvensis L.). The soil was defaunated by heating to 75–80°C for 2 h. Two wireworm larvae were added to each pot. Young greenhouse-grown mustard seedlings in the two-leaf stage were transplanted into each pot. Leaf herbivory of the plants was studied by infesting four leaf plants with two cabbage worms (Pieris rapae L.) (Lepidoptera: Pieridae). Cabbage worms were removed after 30–50% of the leaves were destroyed. The pots were then transferred to a fallow field in summer. Data on plant height and shoot mass, at the beginning and end of the flowering period, were collected for each plant. Fruits and seeds were collected and oven-dried. Insects visiting the flowers were observed for 6 weeks. The experiment was designed to study the effect of leaf herbivory alone, root herbivory alone and both in combination. Plants attacked by root herbivores had a longer flowering period and a higher number of fruits than plants attacked by both herbivores. In plants with both root and leaf herbivores the flowering period was shortened and fewer fruits per plant were produced compared to plants with root herbivory only. Aboveground and belowground herbivores affected plant height, shoot mass, flower physiology, fruit set and even flower visitors. Poveda et al. (2005) conducted a similar experiment to study the effects of decomposers, leaf and root herbivores on mustard (S. arvensis L.) performance with some changes in procedure. Pots used in the experiment were lined with a gauze bag (1 mm mesh) to prevent the escape of soil organisms from pots and colonization by soil macrofauna from outside through drain holes. The soil in pots was defaunated by freezing at −20°C for 3 days. Five grams of grass leaf litter was placed on top of the soil. Two earthworms of the species Octolasion trytaeum were added to decomposer treatments. Five wireworms, Agriotes sp., were added as root herbivore treatments. Greenhouse-grown seedlings in the four-to-six leaf stages were transplanted into pots. One day after transplanting, two third-instar larvae of S. litoralis (Boisduval) (Lepidoptera: Noctuidae) were put on seedlings and left until they consumed 50% of the leaves. The pots were then buried in the field with 3 cm of the upper margin above the soil surface. Several aphids attacked the plants later. Aphid species recorded were Brevicoryne brassicae (L.) (over 70% of species present), Lipaphis erysimi Kalt and Aphis sp., Myzus persicae (Sulzer) and Macrosiphon euphorbiae Thomas (Homoptera: Aphididae). In this

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study, root herbivores did not affect plant biomass. Leaf herbivory caused a shortening of the flowering period because of early flower abortion. Earthworms increased plant biomass. They also increased root/shoot ratio, but only in plants that were not attacked by leaf herbivores. There were combined effects of decomposers and aboveground and belowground herbivores on the aboveground herbivore–parasitoid and plant–pollinator interactions.

1.4.2. Removal of root herbivores: insecticide-based approaches Containers to limit the size and extent of insect infestation are not the only method of studying root herbivory in the field. Maron (1998) manipulated the insect population of ghost moths, Hepialus californicus (Boisduval) (Lepidoptera: Hepialidae), infesting bush lupine (Lupinus arboreus Sims) by insecticide treatment of plants and with the insecticide Sevin (Union Carbide Corporation, Danbury, Connecticut, USA), and plant trunks and soil with Dursban (DowElanco Corporation, Midland, Michigan, USA). Both aboveground and belowground herbivores were suppressed by applying both insecticides to the same plants. Control plants were sprayed with water allowing for natural insect infestations to occur. Dursban was used because of its non-toxic effects on other organisms in the soil such as nitrogen-fixing bacteria, nitrifying and denitrifying bacteria, fungal populations, earthworms and spiders (Masters, 2004). Results showed that Dursban did not affect nodule number or size. Sevin was chosen as the foliar insecticide because of its effectiveness against a wide range of insects and because it had no toxicity to the plant or any effect on ghost moth abundance in lupine roots or trunks. Treatments in the experiment were plots of lupine plants with: (i) reduction of flower and seed-feeding insects; (ii) reduction of root-feeding insects; (iii) suppression of both aboveground and belowground herbivores; and (iv) no herbivore suppression. Results showed that suppression of aboveground herbivores had positive effects on seed pod and total seed production in 2 out of 3 years. Protecting plants from underground herbivores had no effect on seed pods or seed output, but plants protected from both herbivores produced 67% more seeds. The combined negative effect on seed production of aboveground and belowground herbivores was additive. Ghost moth larvae killed many plants after they had set seed. In another study, Strong et al. (1995) recorded that the populations of ghost moths fluctuated, causing plant populations to be patchy. The waxing and waning of the plant population was thought to be due to ghost moth mortality when attacked by entomopathogenic nematodes (Heterorhabditis sp.), which lowered insect pressure on the plant population, allowing it to recover. Care has to be exercised with any destructive procedure, whether it be pot- or core sampling-based, to ensure that a large enough number, a large enough volume and an appropriate distribution are used for the organism under study. In addition, seasonality of movement should be considered,

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such that the depth of coring should be a prime concern when quantifying density of some species of earthworm which migrate through soil horizons in response to change in environmental conditions. Most root feeders have a clumped distribution (Brown and Gange, 1990; Masters, 2004), and any sampling strategy should take this into account. The spatial aggregation of an organism should determine the choice of sampling strategy; for example, with rhizosphere organisms the sampling would have to focus on both rhizosphere and bulk soil locations.

1.5. Non-destructive Field Techniques Non-destructive methods have the advantage that the same position is measured over time, in contrast to destructive measures, where variability of location is included in the measurement. Such methods also permit aspects of root dynamics to be measured. Rhizotrons have been used in the field to study root growth and herbivory.

1.5.1. Large-scale field rhizotrons A rhizotron is a deep trench with a plate of glass against one wall and a roof over the whole structure (Zobel, 1993). Gunn and Cherrett (1993) developed a food-web model from field observations made using a large custom-built rhizotron, which allows the soil ecosystem to be studied under natural conditions without disturbing the animals or their environment. They observed a high degree of omnivory, no clear compartmentation, and separate herbivore and decomposer food webs could not be distinguished. Plant root systems were an important resource for many soil animals. There was evidence that certain taxa fed preferentially on different parts of the root system but there was no clear evidence for exclusive guilds or species packing. Wilson et al. (1995) examined the ability of a large, purpose-built underground observation chamber (rhizotron) to examine the effects of two pesticides on the interactions between soil invertebrates, root growth and aboveground plant production within a grassland ecosystem. The pesticides, Dursban 5Gn and Tornado (Carbaryl), killed most of their target species (soil arthropods and annelids, respectively), but some taxa thrived in pesticidetreated plots, probably due to reduced interspecific competition, decreased predation and/or increased food supply. In arthropod-impoverished (Dursban-treated) plots, the total length of visible root in a selected portion of the soil profile was reduced by 30% increase in aboveground foliar biomass production. In earthworm-impoverished (Carbaryl-treated) plots, the total length of visible root was not significantly different from that in the control plots and the rate of aboveground foliar production was also comparable.

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1.5.2. Mini-rhizotrons Mini-rhizotron systems allow a greater representation to be made of inherent field variability, as they can be replicated across a field area with greater ease than a generally larger rhizotron plate system. Wells et al. (2002) used minirhizotrons to study arthropod populations in soil beneath peach trees. The mini-rhizotrons were clear butyrate observation tubes installed near the trees at a 30° angle. Roots were videotaped at 2- and 4-week intervals with a miniaturized camera system. Insect populations were controlled with chlorpyrifos (DowElanco Corporation, Midland, Michigan, USA). Results indicate that suppression of the insect population around fine roots decreased the risk of root mortality by 59% compared with mortality in control roots. Insecticide treatment also lowered the development of pigmentation of roots, implying that browning may be enhanced by soil insects under natural conditions. Brown roots have a reduced nutrient uptake capacity. Insects which enhance root browning could influence whole plant nutrition and growth without directly removing root tissue. At an upland field site in Scotland, on an established Festuca–Agrostis pasture, the effects of soil amendment on root dynamics, with nitrogen and lime and the regular application of insecticide, were studied using a field mini-rhizotron system (Dawson et al., 2003). The most common insect root herbivore at the site was T. paludosa, and the application of insecticide (chlorpyrifos) reduced numbers of insect larvae of all species. Root biomass, root appearance, root disappearance and root density were all reduced by the insecticide. This reduced rooting could reflect reduced root replacement, due to the reduction in root herbivory in insecticide-treated plots, or could be a direct effect of insecticide application on the roots.

1.5.3. Limitations of field techniques Hunter (2001) points out that root-feeding insects have been greatly understudied. Brown and Gange (1990) indicated that the paucity of ecological studies of belowground herbivores most likely stems from difficulties in sampling and taxonomy of causal agents and assessing the extent of damage. Thirteen years later, Blossey and Hunt-Joshi (2003) believed that root feeders continued to be neglected in studies examining plant behavioural interactions and the influences of herbivory on plant community competition because of the limited availability of appropriate methods. One limitation is that insect root herbivore treatments in pot experiments require a ready supply of standardized root-feeding insects either from a field (e.g. Johnson et al., 2008) or from some standardized rearing technique (e.g. Fisher and Bruck, 2004). Both methods have problems. Restrictions are often caused by limited seasonal windows of opportunity for collection of root feeders. Field collections do not guarantee that the root feeders are of the same species or of the same stage of development (Masters, 2004). Culturing insects ensures that the herbivores are of the same species, are

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genetically similar and are of the same age, but cultures are notoriously difficult to establish and maintain (Masters, 2004). Masters (2004) further points out that exclusion of insects in the field largely involves the use of soil insecticide. One of the main problems with the use of a soil insecticide is that its application invariably involves some sort of contact with aboveground biota, so it can potentially bias results. He recommends granular insecticides that do not stick to foliage, followed by irrigation to wash the insecticide into the soil. Endlweber et al. (2006) used insecticides to suppress Collembola to study Collembolan density and community structure in an early set-aside arable field. The treatments were aimed at studying aboveground and belowground herbivory on plant succession. The study showed that insecticide application strongly affected the structure of the decomposer community. Therefore, results of studies using insecticides to manipulate aboveground and belowground herbivores have to be interpreted with caution because changes in plant growth, plant competition and plant succession may not be exclusively due to reduced damage by herbivores in treated plots, but may be also affected by decomposer-mediated changes in decomposition processes and nutrient cycling by decomposer organisms. The density of insects used in additive manipulation experiments on root herbivory is critical to the results. Too few insects may not have much influence on root biomass or injury. Byers et al. (1996) attracted target insects to an experimental lucerne nursery by planting white clover in the alleys between plots. The white clover was highly attractive to adult Sitona weevils, whose egg-laying activities increased the local population of root-feeding larvae in the lucerne nursery. Most studies that involve adding insects to pots base the numbers used on population estimates of root-feeding herbivores in the natural environment. However, most root feeders have a clumped distribution (Brown and Gange, 1990; Masters, 2004), so numbers used in pots are an average of these field populations and may be biased. Studies with very high numbers, on the other hand, may overemphasize damage, and more reflect responses within patches.

1.6. Recommendations New non-destructive techniques offer an alternative approach for the investigation of root herbivory and, in particular, behavioural interactions of root herbivores. X-ray tomography in the laboratory and acoustic detection in the field (reviewed by Mankin et al., Chapter 2, this volume) offer considerable benefits. However, as Johnson et al. (2007a) discuss, these techniques also have limitations and are best considered as complementary to existing techniques, such as those considered in this chapter. The ready availability and simplicity of many of the techniques discussed in this chapter make them particularly useful for exploratory research, which can then inform experiments that use more specialized equipment such as X-ray tomography and

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acoustic detection. Linking these experimental approaches to mathematical modelling (Johnson et al., 2007a) could be advantageous for efficiently studying and controlling root-feeding herbivores, not least by predicting events such as egg hatching (Johnson et al., 2007b) and movement patterns in the soil (Zhang et al., 2006), which would otherwise remain unseen. In addition to controlling root herbivore pests, Blossey and Hunt-Joshi (2003) suggest that the popularity of root-feeding herbivores in weed control programmes has a good chance of increasing interest in this important field. Such research is important for improved plant productivity, health and for an increased understanding of biodiversity interactions. The future directions and challenges for investigating root-feeding herbivores and their impacts need to be considered within the wider ecosystem, incorporating both aboveground and belowground organisms.

References Baker, P.B. and Byers, R.A. (1977) A laboratory technique for rearing the clover root curculio. Melsheimer Entomological Series 23, 8–10. Bernklau, E.J. and Bjostad, L.B. (1998) Behavioral responses of first-instar western corn root worm (Coleoptera: Chrysomelidae) to carbon dioxide in a glass bead bioassay. Journal of Economic Entomology 91, 444–456. Bezemer, T.M., Wagenaar, R., Van Dam, N.M. and Wackers, F.L. (2003) Interactions between above- and belowground insect herbivores as mediated by the plant defense system. Oikos 101, 555–562. Blossey, B. and Hunt-Joshi, T.R. (2003) Belowground herbivory by insects: influence on plants and aboveground herbivores. Annual Review of Entomology 48, 521–547. Boff, M.I.C., Zoon, F.C. and Smits, P.H. (2001) Orientation of Heterorhabditis megidis to insect hosts and plant roots in a Y-tube sand olfactometer. Entomologia Experimentalis et Applicata 98, 329–337. Brown, V.K. and Gange, A.C. (1990) Insect herbivory below ground. Advances in Ecological Research 20, 1–58. Bryson, H.R. (1929) A method for rearing wireworms (Elateridae). Journal of the Kansas Entomological Society 2, 15–21. Byers, R.A. (1995) Factors affecting rearing of clover root curculio (Coleoptera: Curculionidae)

in cone containers. Journal of Economic Entomology 88, 407–414. Byers, R.A. and Kendall, W.A. (1982) Effects of plant genotypes and root nodulation on growth and survival of Sitona spp. larvae (Coleoptera: Curculionidae). Environmental Entomology 11, 440–443. Byers, R.A., Kendall, W.A., Peaden, R.N. and Viands, D.W. (1996) Field and laboratory selection of Medicago plant introductions for resistance to the clover root curculio (Coleoptera: Curculionidae). Journal of Economic Entomology 89, 1033–1039. Dawson, L.A., Grayston, S.J., Murray, P.J. and Pratt, S.M. (2002) Root feeding behaviour of Tipula paludosa (Meig.) (Diptera: Tipulidae) on Lolium perenne L. and Trifolium repens L. Soil Biology and Biochemistry 34, 609–615. Dawson, L.A., Grayston, S.J., Murray, P.J., Cook, R., Gange, A.C., Ross, J.M., Pratt, S. M., Duff, E.I. and Treonis, A. (2003) Influence of pasture management (nitrogen and lime addition and insecticide treatment) on soil organisms and pasture root system dynamics in the field. Plant and Soil 255, 121–130. Dawson, L.A., Grayston, S.J., Murray, P.J., Ross, J.M., Reid, E.J. and Treonis, A.M. (2004) Impact of Tipula paludosa larvae on plant growth and the soil microbial community. Applied Soil Ecology 25, 51–61.

18 Dobrovsky, T.M. (1954) Laboratory observations on Conoderus vagus Candeze (Coleoptera: Elateridae). The Florida Entomologist 37, 123–131. Endlweber, K., Schadler, M. and Scheu, S. (2006) Effects of foliar and soil insecticide applications on the collembolan community of an early set-aside arable field. Applied Soil Ecology 31, 136–146. Fisher, J.R. and Bruck, D.J. (2004) A technique for continuous mass rearing of the black vine weevil, Otiorhynchus sulcatus. Entomologia Experimentalis et Applicata 113, 71–75. Gange, A.C., Brown, V.K. and Farmer, L.M. (1991) Mechanisms of seedling mortality by subterranean insect herbivores. Oecologia 88, 228–232. Gerard, P.J., Crush, J.R. and Hackell, D.L. (2005) Interaction between Sitona lepidus and red clover lines selected for formononetin content. Annals of Applied Biology 147, 173–181. Gunn, A. and Cherrett, J.M. (1993) The exploitation of food resources by soil mesoinvertebrates and macro-invertebrates. Pedobiologia 37, 303–320. Hunter, M.D. (2001) Out of sight, out of mind: the impacts of root-feeding insects in natural and managed systems. Agricultural and Forest Entomology 3, 3–9. Johnson, S.N. and Gregory, P.J. (2006) Chemically-mediated host-plant location and selection by root-feeding insects. Physiological Entomology 31, 1–13. Johnson, S.N., Gregory, P.J., Murray, P.J., Zhang, X. and Young, I.M. (2004) Host plant recognition by the root-feeding clover weevil, Sitona lepidus (Coleoptera: Curculionidae). Bulletin of Entomological Research 94, 433–439. Johnson, S.N., Crawford, J.W., Gregory, P.J., Grinev, D.V., Mankin, R.W., Masters, G.J., Murray, P.J., Wall, D.H. and Zhang, X.X. (2007a) Non-invasive techniques for investigating and modelling root-feeding insects in managed and natural systems. Agricultural and Forest Entomology 9, 39–46. Johnson, S.N., Zhang, X., Crawford, J.W., Gregory, P.J. and Young, I.M. (2007b) Egg hatching and survival time of soil-dwelling

L.A. Dawson and R.A. Byers insect larvae: a partial differential equation model and experimental validation. Ecological Modelling 202, 493–502. Johnson, S.N., Anderson, A., Dawson, G. and Griffiths, D.W. (2008) Varietal susceptibility of potatoes to wireworm herbivory. Agricultural and Forest Entomology 10, 167–174. Kendall, W.A. and Leath, K.T. (1974) Slantboard culture methods for root observations of red clover. Crop Science 14, 317–320. Lola-Luz, T., Downes, M. and Dunne, R. (2005) Control of black vine weevil larvae Otiorhynchus sulcatus (Fabricius) (Coleoptera: Curculionidae) in grow bags outdoors with nematodes.Agricultural and Forest Entomology 7, 121–126. Maron, J.L. (1998) Insect herbivory above- and belowground: individual and joint effects on plant fitness. Ecology 79, 1281–1293. Masters, G.J. (2004) Below-ground herbivores and ecosystem processes. In: Weisser, W. W. and Siemann, E. (eds) Insects and ecosystem function. Springer, Berlin/Germany, pp. 94–112. Murray, P.J. and Clements, R.O. (1992) A technique for assessing damage to roots of white clover caused by root feeding insects. Annals of Applied Biology 121, 715–719. Murray, P.J. and Hatch, D.J. (1994) Sitona weevils (Coleoptera: Curculionidae) as agents for rapid transfer of nitrogen from white clover (Trifolium repens L.) to perennial ryegrass (Lolium perenne L.). Annals of Applied Biology 125, 29–33. Murray, P.J., Dawson, L.A. and Grayston, S.J. (2002) Influence of root herbivory on growth response and carbon assimilation by white clover plants. Applied Soil Ecology 20, 97–105. Poveda, K., Steffan-Dewenter, I., Scheu, S. and Tscharntke, T. (2003) Effects of belowand above-ground herbivores on plant growth, flower visitation and seed set. Oecologia 135, 601–605. Poveda, K., Steffan-Dewenter, I., Scheu, S. and Tscharntke, T. (2005) Effects of decomposers and herbivores on plant performance and aboveground plant–insect interactions. Oikos 108, 503–510.

Methods for Studying Root Herbivory Quinn, M.A. and Hall, M.H. (1992) Compensatory response of a legume rootnodule system to nodule herbivory by Sitona hispidulus. Entomologia Experimentalis et Applicata 64, 167–176. Rasmann, S. and Turlings, T.C.J. (2007) Simultaneous feeding by aboveground and belowground herbivores attenuates plant-mediated attraction of their respective natural enemies. Ecology Letters 10, 926–936. Rasmann, S., Köllner, T.G., Degenhardt, J., Hiltpold, I., Toepfer, S., Kuhlmann, U., Gershenzen, J. and Turlings, T.C.J. (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434, 732–737. Richmond, D.S., Grewal, P.S. and Cardina, J. (2003) Influence of Japanese beetle Popillia japonica larvae and fungal endophytes on competition between turfgrasses and dandelion. Crop Science 44, 600–606. Stevens, G.N. and Jones, R.H. (2006) Influence of root herbivory on plant communities in heterogeneous nutrient environments. New Phytologist 171, 127–136. Stevens, G.N., Pierson, D.R., Nguyen, K. and Jones, R.H. (2007) Differences between resource patches modify root herbivore effects on plants. Plant and Soil 296, 235–246. Strong, D.R., Maron, J.L., Connors, P.G., Whipple, A., Harrison, S. and Jefferies, R.L. (1995) High mortality, fluctuation in numbers, and heavy subterranean insect

19 herbivory in bush lupine, Lupinus arboreus. Oecologia 104, 85–92. Treonis, A.M., Grayston, S.J., Murray, P.J. and Dawson, L.A. (2005) Effects of root feeding, cranefly larvae on soil microorganisms and the composition of rhizosphere solutions collected from grassland plants. Applied Soil Ecology 28, 203–215. Van Tol, R.W.H.M., Van der Sommen, A.T.C., Boff, M.I.C., van Bezooijen, J., Sabelis, M.W. and Smits, P.H. (2001) Plants protect their roots by alerting the enemies of grubs. Ecology Letters 4, 292–294. Wells, C.E., Glenn, D.M. and Eissenstat, D.M. (2002) Soil insects alter fine root demography in peach (Prunus persica). Plant, Cell and Environment 25, 431–439. Wiese, A.H., Riemenschneider, D.E. and Zalesny, R.S., Jr. (2005) An inexpensive rhizotron design for two-dimensional, horizontal root growth measurements. Tree Planter’s Notes 51, 40–46. Wilson, K., Gunn, A. and Cherrett, J.M. (1995) The application of a rhizotron to study the subterranean effects of pesticides. Pedobiologia 39, 132–143. Zhang, X., Johnson, S.N., Gregory, P.J., Crawford, J.W., Young, I.M., Murray, P.J. and Jarvis, S.C. (2006) Modelling the movement and survival of the root-feeding clover weevil, Sitona lepidus, in the root-zone of white clover. Ecological Modelling 190, 133–146. Zobel, R. (1993) The rhizosphere – a great unknown-column. Agricultural Research 41, 2.

2

New Experimental Techniques for Studying Root Herbivores R.W. MANKIN,1 S.N. JOHNSON,2 D.V. GRINEV3 AND P.J. GREGORY2 1

Center for Medical, Agricultural and Veterinary Entomology, Gainesville, Florida, USA; 2Scottish Crop Research Institute, Dundee, UK; 3University of Abertay Dundee, Dundee, UK

2.1. Introduction Many of the chapters in this volume illustrate the importance that root herbivores play in ecosystem processes in both applied and ecological contexts. In most cases, however, relatively less is known about belowground herbivores than their aboveground counterparts (Brown and Gange, 1990; Hunter, 2001). This is largely because root-feeding herbivores live in the soil, an opaque, tri-phasic medium, which makes them harder to study and perhaps a less perceptible part of terrestrial ecosystems. Conventional methods for studying root herbivores (reviewed by Dawson and Byers, Chapter 1, this volume) have proved successful for unravelling a number of aspects of belowground herbivory, but these techniques frequently still have a ‘black box’ characteristic to them. In this chapter, we focus on recent developments in non-invasive methods for studying root herbivores, both in the field (acoustic detection) and in the laboratory (X-ray tomography). We focus on these two non-invasive techniques because they seem to offer the most potential for investigating root herbivory, based on recent studies using a range of root feeders. Other noninvasive methods for studying subterranean herbivores exist (e.g. telemetric techniques reviewed in brief by Reynolds and Riley, 2002), but detailed studies concerning their usage remain scarce, and are therefore not covered in this chapter. We also restrict ourselves to discussing rootfeeding insects in this chapter because these techniques cannot yet be properly exploited for smaller root herbivores such as nematodes, and are probably inappropriate for larger root herbivores such as rodents. A full glossary of the terms used in the text is given below.

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GLOSSARY Accelerometer

Acoustic detection

Geophone

Gray (Gy)

Hounsfield units

Isotropic voxel Piezoelectric probe

Quasi-monoenergetic X-ray beam

X-ray attenuation X-ray radiography of soils X-ray tomography of soils

X-ray microtomography of soils

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A device that generates an electrical signal proportional to the acceleration of an applied vibration Use of sounds or vibrations produced by incidental movement or communication activities of a hidden target organism to estimate the likelihood that the target is present or absent at a sampled site A device that generates an electrical signal proportional to the velocity of ground movement, used to detect earthquakes or seismic vibrations SI unit of absorbed radiation dose; 1 Gy is the absorption of 1 J of radiation energy by 1 kg of matter Quantitative scale for describing radiodensity. The radiodensity of distilled water at standard pressure and temperature is defined as zero Hounsfield units (HU), while the radiodensity of air under the same conditions is defined as 1000 HU Three-dimensional pixels with faces that are all square (i.e. a cube and not a cuboid) An assembly that combines a piezoelectric sensor, which generates an electric charge when it is stressed, with a pointed blade or rod to detect weak signals produced by target organisms deep in the soil. Usually, the probe is inserted into the soil first, and then the sensor is attached to it Polyenergetic X-ray beam in which the spectrum has one dominant wavelength peak and energy spread in the beam is minimized by means of filtering and/ or particular choice of target in the X-ray gun Quantified penetration of materials by X-ray beams Generation of two-dimensional images by passing X-rays through a thin channel of soil A method of generating a three-dimensional image of the inside of a soil column from a series of two-dimensional X-ray images taken around a single axis of rotation As above, but typically with a much higher resolution and using a smaller sample size

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2.2. Acoustic Detection 2.2.1. Background to acoustic techniques Acoustic technology, with a long history of use for the detection of hidden insect infestations in food and wood, has considerable potential for addressing important questions involving the physiology, behaviour and ecology of root-feeding insects (see review by Johnson et al., 2007). In the last few years, several different types of sensors, including microphones (Mankin et al., 2000; Zhang et al., 2003a), accelerometers (Mankin et al., 2001), piezoelectric probes (Mankin and Lapointe, 2003; Mankin and Fisher, 2007) and geophones (Mankin and Benshemesh, 2006), have been tested successfully in detection and monitoring applications. Microphones and accelerometers provide the most easily interpretable signals in low background noise, but the amplifiers for input from the piezoelectric sensors are inexpensive, and the signals are easily filtered to reduce low-frequency background noise. Geophones are inexpensive and highly sensitive to low-frequency sounds, although the signals may be difficult to interpret in high background noise. Because soil strongly attenuates vibrations above 200 Hz, an underground sensor is exposed to lower levels of mid- to high-frequency background noise than in many open-air environments which can facilitate detection of the low-amplitude, 500–1800 Hz sounds produced by soil insects in agricultural (Mankin et al., 2001), or even urban (Mankin et al., 2002), environments. The same attenuation process, however, restricts detection to distances of only 10–30 cm (Mankin and Lapointe, 2003). When the approximate position of the insect is known, this problem can be reduced for accelerometers and piezoelectric sensors by first inserting a probe of appropriate length close to the insect, and then attaching the sensor to the probe. Larvae of the citrus fruit weevil, Diaprepes abbreviatus L. (Coleoptera: Curculionidae), for example, often feed on the root crown of a citrus tree, which can be accessed by inserting a 30 cm probe about 10 cm from the trunk, pointing slightly inwards (Mankin and Lapointe, 2003). To evaluate spatial distributions of soil insects over large areas, regularly spaced probe assemblies can be multiplexed or monitored continuously, or multiple sites can be monitored over brief periods (e.g. Brandhorst-Hubbard et al., 2001; Mankin et al., 2007). Some insects initially become quiescent when disturbed, but resume activity within 3–5 min. Consequently, it is good practice to monitor over at least a 3-min period after moving from one recording site to another.

2.2.2. Potential applications One type of root herbivory study, for which acoustic technology may be suited but has not yet been applied, is analysis of larval movement within the soil. In this case, sensors could be permanently embedded in a one-, two- or three-dimensional grid before the beginning of the experiment and the larval

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position could be estimated by triangulation or procedures similar to those described in Shuman et al. (1993). These methods would have lower resolution than X-ray tomography (see below), but cover a much greater scale and can be used in the field. Two concerns that have delayed widespread transfer of acoustic technology from research to general agricultural usage involve the complex problems of how best to discriminate insect-produced signals from background noise, and how to interpret the spectral characteristics and temporal patterns of detected insect sounds. Although there is overwhelming interest in completely automated, instrument-based monitoring methods, most of the progress until now has come from combining subjective, listener-based assessments with computer-based assessments of detected signals. In field tests, the output from acoustic sensors inserted at a series of regularly spaced sites is usually assessed in real time by headphones and saved for confirmatory signal-processing analysis on a digital flash memory or tape recorder. To facilitate objective signal processing, examples of independently verified sounds recorded in the same field are screened by experienced listeners to ensure their quality. These signals are then used to construct spectral profiles (Mankin et al., 2000) against which a computer program compares all of the sounds recorded at each monitoring site. Sounds that adequately match the profiles are judged to be valid insect sounds and sounds that do not match are discarded as background noise. To assess the likelihood that an insect infestation is present at a given site, the computer program sets the values of discrete indicator variables by comparing the rates of valid sounds against threshold sound-rate criteria (Mankin et al., 2007). For example, a low likelihood of infestation might be specified if the rate is 20 sounds min−1. This procedure yields assessments approximating to those of experienced listeners who classify sites into discrete categories (e.g. high, medium or low likelihood of infestation), based on the rate and quality of detected sounds. In addition to their utility in assessing infestations at monitoring sites, acoustic indicator variables also can be used in geostatistical and clustering analyses (Perry and Dixon, 2002) to spatially quantify soil insect populations (Mankin et al., 2007).

2.2.3. Linking sounds with root herbivore behaviour Some limited progress has been made in the development of techniques to identify different types of sounds and relate them to behavioural activities, primarily through analyses of sound durations and temporal patterns. In assessments of sounds produced by white grubs Phyllophaga spp. (Zhang et al., 2003b), short (2 cm long in the case of Harrison et al., 1993). This limitation represented a serious obstacle, since the early stages of most root-feeding insects are considerably smaller than 2 cm. However, with the development of devices that could scan soil columns at higher resolution and with minimal energy dosage (e.g. Gregory et al., 2003; Jenneson et al., 2003), it became possible to consider using these techniques for studying much smaller rootfeeding insects. The use of X-ray tomography, and in particular X-ray microtomography, for studying root-feeding insects has been employed most recently for studying the soil-dwelling larvae of the clover root weevil (Sitona lepidus), a serious pest of white clover (Trifolium repens L.). The soil-dwelling stages cause most damage to the plant, particularly when the newly hatched (or neonatal) larvae attack root nodules that house N2-fixing Bradyrhizobium bacteria (Gerard, 2001). In a series of laboratory experiments, Johnson et al. (2004b) demonstrated that S. lepidus larvae burrowed

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Fig. 2.2. X-ray tomographic images of root-feeding insects. The sequential movement of neonatal Sitona lepidus larvae through the soil towards the lower clover Bradyrhizobium root nodule, with locations shown at: (i) 0 h, larva unseen at soil surface; (ii) 3 h; (iii) 6 h; and (iv) 9 h. White bar = 10 mm. (From Johnson et al., 2004b. Reproduced with permission.)

between 9 and 27 mm in 9 h towards nodules on white clover roots at a mean speed of 1.8 mm h−1 (Fig. 2.2). Burrowing patterns were usually convoluted rather than linear, with changes in trajectory evident from this study that would be masked in more commonly used ‘slant boards’ (see Dawson and Byers, Chapter 1, this volume). When larvae were given a choice of host plants, S. lepidus larvae showed a statistically significant preference for white clover roots over soil, grass or two other legumes; however, there was no significant difference in the rate of movement to roots of the different plant species (Johnson et al., 2004a). These measurements of rates of movement and trajectory have been incorporated into an individual-based lattice Boltzmann model to simulate the movement of individual larvae (Zhang et al., 2006).

2.3.3. Case study: using X-ray microtomography to study wireworm herbivory within potato tubers A field trial by Johnson et al. (2008) demonstrated that Agriotes spp. wireworms (the juvenile stages of click beetles) showed differential patterns of herbivory on tubers of different potato varieties. Here, we show that X-ray tomography can be used to study the localized feeding behaviour of the insect within a tuber. Seven potato tubers (cv. Marfona – one of the most susceptible varieties; Johnson et al., 2008) of similar appearance and size (c.35–40 mm diameter × 40–45 mm length) were used for this study (supplied by Scottish Agronomy Ltd., Kinross, UK). Single wireworms were placed inside seven plastic tubes (20 mm diameter × 50 mm length) that

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were closed at one end and had been filled to capacity with 11.7 g of soil (sieved 50%; in other words, they had consumed the majority of the tissue within the region of interest (tissue consumed ranged from 154 to 3016 mm3). This example shows how X-ray tomography can be used to identify regions of localized feeding within a tuber and to quantify the amount of tissue consumed by wireworms over time. The exact chemical and physical properties of potato tubers that affect wireworm herbivory remain unclear (Johnson et al., 2008), although sugars and glycoalkaloids are thought to promote and deter feeding activity, respectively (Jonasson and Olsson, 1994). X-ray tomography could be a particularly useful tool for determining the effects of these chemicals on wireworms. For instance, by non-invasively observing feeding within tubers it may be possible to determine whether wireworms feed on parts of the tuber containing particular compounds in specific concentrations.

2.3.4. New developments in X-ray tomography for studying root herbivores Recently, commercial instruments have become available to investigate biological materials in a soil medium, including root-feeding insects. Johnson et al. (2007) describe an X-ray tomography system (supplied by X-TEK Group, UK), which has been used to obtain images of a mature wireworm (Agriotes sp. L. Coleoptera: Elateridae) in cross section (Fig. 2.3B) and a neonatal vine weevil, Otiorhynchus sulcatus Fabricius (Coleoptera: Curculionidae) (Fig. 2.3C). This system has a 5 µm focal spot reflection target (different targets can be used, including tungsten, molybdenum, copper and silver) and an X-ray source operating at 25–160 kV and 0–1000 µA (non-continuous). The device can be used for scanning a maximum area of soil of 20 × 20 cm, weighing up to 2 kg, which represents a significant advance on previously used apparatus. Despite this improvement, a major limitation associated with X-ray tomography remains the trade-off between scanning time, resolution of images, radiation dosage and the size of the experimental arena. Larger arenas usually involve increased exposure of the subject to higher energy sources and produce lower resolution images. These considerations must be balanced by researchers when addressing specific experimental goals (Johnson et al., 2007) and will dictate to a large extent what can be achieved.

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X-ray tomography apparatus can be custom-made (e.g. Jenneson et al., 2003), but the recent availability of commercial bench-top units, which can be purchased relatively inexpensively, means that this technique is now available to more researchers. The comparative ease with which these units can be operated, together with improvements in resolution and scanning time, has made X-ray tomography much more attractive for investigating the behaviour of root-feeding insects in the soil.

2.4. Conclusions Interest in root herbivory is likely to increase as applied and ecological researchers recognize the important role such herbivores play in terrestrial ecosystems. Research in this area has been undoubtedly frustrated by the difficulty in observing and accessing root herbivores, but the techniques discussed here provide at least some scope for addressing these issues. Acoustic detection techniques are non-invasive and have demonstrated applications for the detection of root herbivores in field and container crops. As acoustic signal-processing software becomes more sophisticated, acoustic techniques are likely to be developed to analyse movement and feeding behaviour in greater detail. However, interference from background noise and the limited range of acoustic signals in soil will limit the monitoring range of acoustic devices to 10–30 cm for the foreseeable future. As previously outlined, the main problem in using X-ray tomography for studying root-feeding insects is the trade-off that exists between sample size, the resolution of insects and roots, scanning time and permissible energy dosage. Ideally, researchers would like to be able to have sufficiently large experimental arenas (i.e. larger sample sizes), while obtaining detailed images of the insect–root interactions relatively rapidly (preferably real time) and exposing the organisms to minimal amounts of energy. Meeting these requirements poses a challenge, but the technology is developing rapidly. A combination of reduced focal spot diameter of the source, finer detectors assembled in larger detector arrays and improved data handling and image reconstruction software should permit imaging of samples at temporal and spatial scales to be biologically useful.

Acknowledgements The authors would like to extend their thanks to Deborah Hutchison, Derek Read (University of Reading) and Eric Anderson (Scottish Agronomy Ltd.) for assistance with aspects of this research. Scott N. Johnson and Peter J. Gregory acknowledge the support of the Scottish Government Rural and Environment Research and Analysis Directorate (RERAD) for SCRI. Dimitri V. Grinev acknowledges the support of BBSRC and RCUK. Richard W. Mankin thanks Peter Samson and Keith Chandler for assistance with aspects of this research and acknowledges partial support from BSES Ltd.

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Hunter, M.D. (2001) Out of sight, out of mind: the impacts of root-feeding insects in natural and managed systems. Agricultural and Forest Entomology 3, 3–9. Jenneson, P.M., Gilboy, W.B., Morton, E.J. and Gregory, P.J. (2003) An X-ray microtomography system optimised for the lowdose study of living organisms. Applied Radiation and Isotopes 58, 177–181. Johnson, S.N., Gregory, P.J., Murray, P.J., Zhang, X. and Young, I.M. (2004a) Host plant recognition by the root-feeding clover weevil, Sitona lepidus (Coleoptera: Curculionidae). Bulletin of Entomological Research 94, 433–439. Johnson, S.N., Read, D.B. and Gregory, P.J. (2004b) Tracking larval insect movement within soil using high resolution X-ray microtomography. Ecological Entomology 29, 117–122. Johnson, S.N., Crawford, J.W., Gregory, P.J., Grinev, D.V., Mankin, R.W., Masters, G.J., Murray, P.J., Wall, D.H. and Zhang, X.X. (2007) Non-invasive techniques for investigating and modelling root-feeding insects in managed and natural systems. Agricultural and Forest Entomology 9, 39–46. Johnson, S.N., Anderson, A., Dawson, G. and Griffiths, D.W. (2008) Varietal susceptibility of potatoes to wireworm herbivory. Agricultural and Forest Entomology 10, 167–174. Jonasson, T. and Olsson, K. (1994) The influence of glycoalkaloids, chlorogenic acid and sugars on the susceptibility of potato tubers to wireworm. Potato Research 37, 205–216. Mankin, R.W. and Benshemesh, J. (2006) Geophone detection of subterranean termite and ant activity. Journal of Economic Entomology 99, 244–250. Mankin, R.W. and Fisher, J.R. (2007) Acoustic detection of Otiorhynchus sulcatus (Fabricius) (Coleoptera: Curculionidae) larval infestations in nursery containers. Oregon State University Agricultural Experiment Station Special Report 1065, 10–15. Mankin, R.W. and Lapointe, S.L. (2003) Listening to the larvae. Acoustic detection

32 of Diaprepes abbreviatus (L.). Proceedings of the Florida State Horticultural Society 116, 304–308. Mankin, R.W., Brandhorst-Hubbard, J., Flanders, K.L., Zhang, M., Crocker, R.L., Lapointe, S.L., McCoy, C.W., Fisher, J.R. and Weaver, D.K. (2000) Eavesdropping on insects hidden in soil and interior structures of plants. Journal of Economic Entomology 93, 1173–1182. Mankin, R.W., Lapointe, S.L. and Franqui, R.A. (2001) Acoustic surveying of subterranean insect populations in citrus groves. Journal of Economic Entomology 94, 853–859. Mankin, R.W., Osbrink, W.L., Oi, F.M. and Anderson, J.B. (2002) Acoustic detection of termite infestations in urban trees. Journal of Economic Entomology 95, 981–988. Mankin, R.W., Hubbard, J.L. and Flanders, K.L. (2007) Acoustic indicators for mapping infestation probabilities of soil invertebrates. Journal of Economic Entomology 100, 790–800. Perry, J.N. and Dixon, P.M. (2002) A new method to measure spatial association for ecological count data. Ecoscience 9, 133–141. Pierret, A., Capowiez, Y., Moran, C.J. and Kretzschmar, A. (1999) X-ray computed tomography to quantify tree rooting spatial distributions. Geoderma 90, 307–326. Rauth, S.J. and Vinson, S.B. (2006) Colony wide behavioral contexts of stridulation in imported fire ants (Solenopsis invicta Buren). Journal of Insect Behavior 19, 293–304. Reynolds, D.R. and Riley, J.R. (2002) Remotesensing, telemetric and computer-based technologies for investigating insect movement: a survey of existing and potential techniques. Computers and Electronics in Agriculture 35, 271–307. Shuman, D., Coffelt, J.A., Vick, K.W. and Mankin, R.W. (1993) Quantitative acoustical detection of larvae feeding inside kernels of grain. Journal of Economic Entomology 86, 933–938.

R.W. Mankin et al. Villani, M.G. and Gould, F. (1986) Use of radiographs for movement analysis of the corn wireworm, Melanotus communis (Coleoptera: Elateridae). Environmental Entomology 15, 462–464. Villani, M.G. and Nyrop, J.P. (1991) Agedependent movement patterns of Japanese beetle and European chafer (Coleoptera: Scarabeidae) grubs in soil turfgrass microcosms. Environmental Entomology 20, 241–251. Villani, M.G. and Wright, R.J. (1988) Use of radiography in behavioral studies of turfgrass-infesting scarab grub species (Coleoptera L. Scarabaeidae). Bulletin of the Entomological Society of America 34, 132–144. Yack, J.E., Smith, M.L. and Weatherhead, P.J. (2001) Caterpillar talk: Acoustically mediated territoriality in larval Lepidoptera. Proceedings of the National Academy of Sciences of the United States of America 98, 11371–11375. Young, I.M., Crawford, J.W. and Rappoldt, C. (2001) New methods and models for characterising structural heterogeneity of soil. Soil and Tillage Research 61, 33–45. Zhang, M., Crocker, R.L., Mankin, R.W., Flanders, K.L. and Brandhorst-Hubbard, J.L. (2003a) Acoustic estimation of infestations and population densities of white grubs (Coleoptera: Scarabaeidae) in turfgrass. Journal of Economic Entomology 96, 1770–1779. Zhang, M.L., Crocker, R.L., Mankin, R.W., Flanders, K.L. and Brandhorst-Hubbard, J.L. (2003b) Acoustic identification and measurement of activity patterns of white grubs in soil. Journal of Economic Entomology 96, 1704–1710. Zhang, X., Johnson, S.N., Gregory, P.J., Crawford, J.W., Young, I.M., Murray, P.J. and Jarvis, S.C. (2006) Modelling the movement and survival of the root-feeding clover weevil, Sitona lepidus, in the root-zone of white clover. Ecological Modelling 190, 133–146.

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Root Feeders in Context

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3

Root Herbivory in Agricultural Ecosystems R.P. BLACKSHAW1 AND B.R. KERRY2 1

The University of Plymouth, Devon, UK; 2Rothamsted Research, Harpenden, UK

3.1. Introduction Root herbivory is of considerable economic importance in agriculture, with many of the more intractable pest species feeding in the soil. Consideration of root herbivory in grasslands is given elsewhere (see Seastedt and Murray, Chapter 4, this volume) and we will focus on arable and horticultural crops, with a particular emphasis on the UK as a region. In essence, an agricultural system at the scale of individual fields is a series of time-bound monocultures that form a rotation. This provides the temporal scale within which to consider root herbivores, but there is also a spatial scale that arises out of the suitability of different geographic regions for different cropping systems. As a result, arable farming is more important on the eastern side of the country; large-scale vegetable production has centres in Cornwall, Lancashire and Lincolnshire. Also, the within-field spatial scale is limited for soil pests, which are usually highly aggregated. For example, most nematodes occur as inbred populations within patches that extend by 25 years. As with all parasites, large numbers of individuals fail to survive during the transmission phase in their life cycles because they fail to find a suitable host. This is especially true for nematodes that are confined to the labyrinth of macro-pores in soil. To increase the chances of successful transmission, despite the limited host range of PCN (only some members of the Solanaceae), they have evolved mechanisms to reduce the hatch of eggs in the absence of plant hosts and to increase the chances of infective juveniles locating host roots. Roots of potato plants release diffusates that induce the eggs to hatch and second-stage infective juveniles (J2) emerge and migrate towards the root. The complex terpene, solanoeclipin, is a signalling compound that induces the J2 to hatch (Mulder et al., 1992) and root diffusates generally alter the surface coat of the infective juveniles in preparation for their parasitic phase within host roots. The infective juvenile invades just behind the root tip in the zone of elongation and migrates intracellularly towards the stele by cutting its way through the cortical cells with its stylet. It establishes a specialized feeding cell, a syncytium, in the pericycle, cortex or endodermis. This feeding cell is multi-nucleate and represents a series of cells that coalesce as a result of protoplast fusion through widening plasmodesmata and the breakdown of adjacent cell walls. The syncytia are metabolically active and contain dense cytoplasm in which the smooth endoplasmic reticulum, mitochondria, ribosomes and plastids proliferate and the vacuole is much reduced; the cell walls have finger-like projections that greatly increase the surface area and support rapid transfer from the plant’s conducting tissue to the developing nematode.

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The invasion of infective juveniles, their migration to the feeding site and the establishment of the feeding cell have profound influences on gene expression and the physiology of the host. Pathogenesis-related proteins are released and may be found in the leaves of infected plants days after nematode invasion – an indication of the host mounting its defence to attack by other pathogens (Hammond-Kosack et al., 1989). There is no evidence that production of these proteins affects nematodes directly. A number of potential virulence factors have been identified in the saliva of cyst nematodes (Gao et al., 2003), but the key factors in the formation of feeding cells remain unclear. If the feeding cell fails to form, the nematode dies and this is the basis of the resistant reaction. The expression of several hundred genes is either up- or down-regulated in cyst nematode-infected roots (Ithal et al., 2007) and the identification of key genes involved in the host–parasite interaction is challenging, especially as some may be only briefly expressed. However, genetic modifications, which inhibit specific proteinases produced by feeding nematode females, have demonstrated potential for the creation of new resistant cultivars (Urwin et al., 2001). The developing juvenile nematode feeds continuously from the syncytium, moults three times to become a saccate female that expands and ruptures the root cortex and is exposed in the rhizosphere. Adult males emerge from roots to fertilize females, which produce around 400 eggs before their bodies tan to form the resistant cysts that remain in soil. PCN are univoltine and amphimictic, but small infestations may increase >100-fold in a growing season. However, multiplication rates are usually much less because intraspecific competition causes a switch in the sex ratio in favour of developing males, which provides a feedback mechanism on population growth, as resources become limited in heavily infected roots (Trudgill, 1967). Approximately 30% of the eggs hatch each year in the absence of a host plant, but this decline rate is highly variable between nematode populations and soil conditions. Although a wide range of soil factors affect the activity of nematodes and their damage to crops, in most agricultural soils in which pH is regulated and nutrients supplied, temperature and soil moisture are the principal abiotic factors affecting nematode dynamics (Barbercheck and Duncan, 2004). A wide range of natural enemies have been identified that may compete, parasitize, predate and antagonize different stages of PCN, and some soils that are suppressive due to the activities of nematophagous fungi have been identified (Crump and Flynn, 1995). However, the impact of natural enemies on PCN dynamics, including the decline of populations between host crops, is poorly understood. Although PCN is an introduced pest to Europe from Latin America (Turner and Evans, 1998) natural enemies are present in UK soils that may be increased in experimental conditions to population densities that significantly reduce PCN multiplication (Crump, 1998).

3.3.2. Damage to crops by potato cyst nematodes As with most nematode damage, PCN do not cause characteristic symptoms aboveground. Heavily infested plants occur in patches of stunted and some-

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times chlorotic plants and are often confused with plants suffering from soil compaction, waterlogging or poor nutrition. Invasion of roots by large numbers of second-stage juveniles of PCN causes root elongation to slow and, in the case of large infections, growth ceases. These nematodes profoundly affect root architecture, function and infested root systems are more branched and more superficial in the soil profile compared to healthy root systems. Nematode-infested plants are therefore more subject to moisture stress and reduced nutrient uptake, which in turn affects the rate of photosynthesis, rate of growth and plant biomass. Female cyst nematodes require about 40 times more resources than males during their development and it is clear that the syncytium is a sink for plant nutrients. However, even in the much-studied cyst nematodes, the mechanism by which pest species cause plant damage and reduce yields is still not clear and there is considerable debate as to the relative importance of changed root architecture and direct feeding damage. Trudgill et al. (1975) observed differences in haulm growth only 4–5 weeks after planting, which suggested that the main effects of PCN on potatoes were caused by invading juveniles affecting root growth and not by egg-producing females that occurred later in the season. Large infestations of the cereal cyst nematode, H. avenae, caused about 20% more yield loss in susceptible lines in which female nematodes developed, compared to near-isogenic resistant lines in which no females were produced (Cotten, 1967), indicating significant effects of female feeding damage, as the roots of both lines were similarly invaded by the nematode. However, there was an approximately twofold difference in the yields achieved on a lightly infested soil, compared to a heavily infested soil, suggesting that differences in nematode invasion of roots may have a much greater effect on overall yields than female feeding damage. Trudgill et al. (1975) estimated that about 5% of total plant nitrogen was found in female PCN in heavily infested plants and suggested that female feeding may account for 40–50% of the yield loss (Trudgill et al., 1998). It is clear, however, that cyst nematode damage to crops is densitydependent and can be predicted from the pre-cropping nematode egg count in soil (Fig. 3.3). At low nematode densities plants are able to compensate for reduced root development and there is no significant damage until the threshold (T) is exceeded. Thereafter, yields decrease with increased nematode infestation until a minimum yield is reached; nematode parasitism rarely kills plant hosts. The tolerance threshold has been estimated to be 1–2 eggs g soil−1 for both G. pallida and G. rostochiensis, but this threshold differs significantly for different biotic and abiotic conditions. Yield losses are greater in sandy than in organic soils and in dry compared to wet years. Yield losses of 2.3–2.8 t ha−1 for every 20 eggs g soil−1 are typical (Whitehead, 1995). The negative relationship between the initial population in soil > T and yield is linear and can be estimated by regression analysis; there are significant differences in the slope of the relationship due to cultivar (Fig. 3.4), which differ in their tolerance to nematode attack. Tolerance is associated with rapid root growth, which may enable plants to support greater nematode reproduction, especially at large infestation levels. Similarly, damage caused by PCN may be alleviated by addition of fertilizer, which by providing more nutrients makes plants more tolerant to

46

R.P. Blackshaw and B.R. Kerry Crop damage becomes significant above this threshold density

Percentage yield

100 80

Yield decreases as nematode numbers increase

60

Yield loss reaches maximum

40 20 T

0 1

10 100 1000 10,000 Initial population density (eggs/g soil)

Fig. 3.3. Relationship between pre-cropping nematode population density and crop yield. (After Seinhorst, 1965.) Y = m + (1 − m)zP − T where Y = yield; m = minimum yield; T = tolerance limit; z is a constant (10 years to decrease to levels below the damage threshold; this slow natural decline rate requires interventions to limit yield losses and decrease nematode multiplication on the crop. G. pallida is now the dominant species of PCN in potato land in England and Wales and is proving much more difficult to control than G. rostochiensis for three main reasons. First, populations of G. pallida are more genetically diverse than those of G. rostochiensis; all populations of G. rostochiensis are controlled by the H1 gene in cultivars such as Maris Piper but there are only sources of partial resistance available to G. pallida, which select more virulent populations of this species (Turner, 1990). Second, eggs of G. pallida often hatch at a slower rate and the juveniles remain viable in soil for longer than those of G. rostochiensis; hence, control using nematicides applied at planting may be less effective as the infective juveniles of G. pallida are active in soil for a longer period than those of the other species. Third, G. pallida population decline rates between potato crops are less and longer crop rotations are needed to reduce populations to

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non-damaging levels than for G. rostochiensis; hence, these two sibling species that were only distinguished for the first time in 1973 have very different biology that significantly affects their management. Chemical control of soil pests is often expensive and this is particularly true for nematode control. Some growers on land heavily infested with PCN apply a fumigant, which is a general soil biocide, in the autumn and a non-fumigant, granular carbamate or organophosphate before planting, at a cost of about £900 ha−1. Most growers rely on non-fumigant nematicides, which are easier to manage and do not require seedbed preparation in the autumn, but patch application of fumigants could reduce costs while maintaining high levels of control (Evans et al., 2003). In general, however, nematicides are some of the most toxic compounds used in agriculture and several have already been banned and removed from the market. Alternative methods for the management of PCN are urgently needed but, to date, have proved difficult to develop. The use of trap crops, which are invaded by the nematode but destroyed before the developing female nematodes have matured and produced the next generation of eggs, may reduce populations by 50% (Halford et al., 1999). However, there must be an opening in the rotation to include such crops and it is essential that the crop is harvested within 40–50 days or some nematode females may mature and produce eggs. G. pallida has a temperature threshold of 4°C and requires 450 day degrees above that threshold to complete its development, which can be accurately recorded on a temperature probe in the field and accessed remotely. However, unreliable weather in the autumn may prevent trap crops being destroyed. To reduce the risk of nematode population increase on trap crops a resistant wild Solanum sp., Solanum sisymbriifolium, the roots of which are invaded by the nematode but the infective juveniles have failed to mature, shows considerable promise as a new control measure and its seed is commercially available. The life cycle of PCN with its close dependence on the host plant offers a number of opportunities for new approaches to its management. Research to identify the signals that infective juveniles use to locate host roots and sites for feeding cells (Akhkha et al., 2004), the pheromones that males use to locate females on the root surface (Riga et al., 1996), the identification of new resistance genes with wider activity against G. pallida, the triggers that determine the sex of developing juveniles and the interactions between PCN and rhizosphere and endophytic microorganisms (Kerry, 2000) may provide new genetic and chemical interventions. Currently, the genomes of the root-knot nematodes Meloidogyne hapla (Chitwood) (Tylenchina: Heteroderidae) and M. incognita and the PCN G. pallida are being sequenced, which will provide much new valuable information on the genes required by nematodes to live in soil and by comparison with the free-living Caenorhabditis elegans (Maupas) (Rhabditida: Rhabditidae) help identify genes associated with root herbivory. Such knowledge may provide a step change in the options for the sustainable management of PCN, but it could be 20 years before these are developed into practical measures to be used by the grower.

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3.4. Conclusions Soil pests and diseases provide significant management problems because they are often difficult to access and are spread within a huge bulk of soil (2500 t ha−1). As a consequence, application rates of pesticides may be much greater than those used to control pests aboveground. The value of the crop is the determinant of the economic viability of this approach and so the majority of treatments against soil pests in arable systems occurs in vegetables. This is by no means a universal dictum; species such as T. paludosa which are frequent on the surface at night are as sensitive to insecticides as many foliar pests. Nevertheless, such intensive use of pesticides in soil that is increasingly recognized as an essential habitat to sustain farmland biodiversity is, arguably, unsustainable in the long term. While there are a range of generic alternative approaches to pesticides that have been developed in pest management, their application to soil pests has to be considered differently according to the groups defined earlier in this chapter. The spatio-temporal focus of these alternatives for Group 1 pests lies in rotations. As we have shown for leatherjackets, much of the knowledge needed to manage populations is now in place. The same cannot be argued for other species in the group; we have partial knowledge about slugs though less about wireworms. The persistence of PCN makes rotational management problematic because the demand side of the production equation requires potatoes to be grown more frequently than can prevent population build-up. For Group 3 species, the interaction with the host plant is more likely to be a productive research direction. Group 2 pest species present a different sort of challenge. Altering rotations can only have a limited impact on species that have dispersal ranges spanning several fields. If overall population pressure is to be reduced, then this will require management intervention at the landscape scale and considerable changes in behaviour of farm decision makers. It is more realistic to consider how best to reduce oviposition burdens through impeding adult behaviour. Alterations to plant biochemistry to reduce attractiveness provide one possibility. Biopesticides provide a more environmentally benign alternative to nonorganic insecticides, and here differences between the three groups are again apparent. Both Groups 1 and 2 will be best controlled by the application of additional natural enemies (inundation) to the soil habitat. By contrast, Group 3 species are more likely to be susceptible to a conservation biocontrol approach through enhanced habitats for natural enemies. Root herbivory in agricultural systems is a process of continuous interaction between species biology, agronomy and decision making expressed as a rotation. The degree to which different species are prevalent varies with geography and landscape, but collectively they present one of the most intractable challenges to modern agriculture. The study of organisms that inhabit cryptic environments such as the soil presents many challenges in terms of understanding their biology and ecology. These challenges are met through the filter of crop damage symp-

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toms. Thus, research on PCN is much more concerned with interactions with the host plant than are studies on leatherjackets, which have tended towards investigations at larger spatial scales. What should not be overlooked, however, is that the persistence of root herbivory as an economic problem has generated important data on many species that are comparatively immobile. Time series data, in particular, have much to offer broader ecological study because of the relatively low importance of emigration and immigration in comparison with mortality and natality. Both the Group 1 (leatherjackets) and Group 3 (PCN) pests discussed are slow to build up in soil and their relative immobility enables them to be managed on an individual farm or field basis, respectively. Their population dynamics are rarely affected by emigration and immigration and may be more predictable than those pests aboveground or those in Group 2. Hence, decision support systems that predict the outcomes of management procedures are being developed to underpin sustainable crop protection practices, but they require further refinement before they provide practical benefits. These soil pests require more than one control measure to prevent significant damage to crops, and their future management will require the precise integration of such measures, which may be applied at intervals in the rotation and not only to the susceptible crop.

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Root Herbivory in Agricultural Ecosystems Blackshaw, R.P. and Petrovskii, S.V. (2007) Limitation and regulation of ecological populations: a meta-analysis of Tipula paludosa field data. Mathematical Modelling of Natural Phenomena 2, 46 – 62. Blackshaw, R.P. and Vernon, R.S. (2006) Spatiotemporal stability of two beetle populations in non-farmed habitats in an agricultural landscape. Journal of Applied Ecology 43, 680–689. Blackshaw, R.P. and Vernon, R.S. (2008) Spatial relationships between two Agriotes click-beetle species and wireworms in agricultural fields. Agricultural and Forest Entomology 10, 1–11. Blackshaw, R.P., Stewart, R.M., Humphreys, I.C. and Coll, C. (1994) Preventing leatherjacket damage in cereals. Association of Applied Biologists Conference on Sampling to Make Decisions. Cambridge, pp. 189–196. Blaxter, M.L. (2003) Nematoda: genes, genomes and the evolution of parasitism. Advances in Parasitology 54, 101–195. Coll, C., Greenhorn, J.G. and Blackshaw, R.P. (1993) The influence of oilseed rape (Brassica napus) on the occurrence of leatherjackets (Tipula spp.) in winter cereals. Proceedings of Crop Protection in Northern Britain. The Association for Crop Protection in Northern Britain, Dundee, pp. 79–84. Cotten, J. (1967) A comparison of cereal root eelworm resistant and susceptible spring barley genotypes at two sites. Annals of Applied Biology 59, 407–413. Coulson, J.C. (1962) The biology of Tipula subnodicornis Zetterstedt, with comparative observations on Tipula paludosa Meigen. Journal of Animal Ecology 31, 1–21. Crump, D.H. (1998) Biological control of potato and beet cyst nematodes. In: Dale, M.F.B., Dewar, A.M., Fisher, S.J., Haydock, P.P.J., Jaggard, K.W., May, M.J., Smith, H.G., Storey, R.M.J. and Wiltshire, J.J.J. (eds) Protection and Production of Sugar Beet and Potatoes. Association of Applied Biologists, Cambridge, pp. 383–386. Crump, D.H. and Flynn, C.A. (1995) Isolation and screening of fungi for the biological control of potato cyst nematodes. Nematologica 41, 628–638. Evans, K. (1987) The interactions of potato cyst nematodes and Verticillium dahliae on

51 early and maincrop potato cultivars. Annals of Applied Biology 110, 329–339. Evans, K. (1993) New approaches for potato cyst nematode management. Nematropica 23, 221–231. Evans, K., Webster, R., Barker, A., Halford, P. and Russell, M. (2003) Mapping infestations of potato cyst nematodes and the potential for spatially varying application of nematicide. Precision Agriculture 4, 149–162. Ferris, H. (1982) The role of nematodes as primary consumers. In: Freckman, D.W. and Wallwork, J.A. (eds) Nematodes in Soil Ecosystems. University of Texas Press, Austin, Texas, pp. 3–13. French, N. (1969) Assessment of leatherjacket damage to grassland and economic aspects of control. Proceedings of the 5th British Insecticide and Fungicide Conference, Brighton, UK, pp. 511–521. Gao, B.L., Allen, R., Maier, T., Davis, E.L., Baum, T.J. and Hussey, R.S. (2003) The parasitome of the phytonematode Heterodera glycines. Molecular Plant–Microbe Interactions 16, 720–726. Halford, P.D., Russell, M.D. and Evans, K. (1999) Use of resistant and susceptible potato cultivars in the trap cropping of potato cyst nematodes, Globodera pallida and G. rostochiensis. Annals of Applied Biology 134, 321–327. Hammond-Kosack, K., Atkinson, H.J. and Bowles, D.J. (1989) Systemic changes in the composition of the leaf apoblast following root infection with the cyst nematode Globodera rostochiensis. Physiological and Molecular Plant Pathology 35, 495–506. Ithal, N., Recknor, J., Nettleton, D., Hearne, L., Maier, T., Baum, T.J. and Mitchum, M. G. (2007) Parallel genome-wide expression profiling of host and pathogen during soybean cyst nematode infection of soybean. Molecular Plant–Microbe Interactions 20, 293–305. Jones, F.G.W. (1980) Some aspects of the epidemiology of plant parasitic nematodes. In: Kranz, J.P.J. (ed.) Proceedings of the Session on Comparative Epidemiology, 3rd International Congress of Plant Pathology. Centre for Agricultural Publishing and

52 Documentation, Munich, Germany, pp. 71–92. Kerry, B.R. (2000) Rhizosphere interactions and the exploitation of microbial agents for the biological control of plant-parasitic nematodes. Annual Review of Phytopathology 38, 423–441. LaCroix, E.A.S. and Newbold, J.W. (1968) Autumn treatments against leatherjackets. Plant Pathology 17, 78–82. Laughlin, R. (1967) Biology of Tipula paludosa – growth of the larva in field. Entomologia Experimentalis et Applicata 10, 52–68. Maercks, H. (1941) Untersuchungen uber wiesenschnaken. Mitteilungen Biologische Reichsanstaltfür Land Und- Forstwirt Schaft 63, 96–97. Maercks, H. (1953) Über den Massenwechsel von Tipula paludosa Meig. In den Jarhen 1918–1953 und seine Abhangigkeit von der Witterung. Nachrichtenbladt des Deutschen Pflanzenschutzdienstes 5, 177–181. Marks, R.J. and Brodie, B.B. (1998) Potato Cyst Nematodes: Biology, Distribution and Control, 1st edn. CAB International, Wallingford, UK. Mayor, J.G. and Davies, M.H. (1976) Survey of leather-jacket populations in southwest England, 1963–74. Plant Pathology 25, 121–128. Meats, A. (1967a) Relation between soil water tension and rate of development of eggs of Tipula oleracea and T. paludosa (Diptera: Nematocera). Entomologia Experimentalis et Applicata 10, 394–400. Meats, A. (1967b) Relation between soil water tension and growth rate of larvae of Tipula oleracea and T. paludosa (Diptera) in turf. Entomologia Experimentalis et Applicata 10, 312–320. Milne, A., Laughlin, R. and Coggins, R.E. (1965) The 1955 and 1959 population crashes of the leatherjacket, Tipula paludosa Meigen, in Northumberland. Journal of Animal Ecology 34, 529–534. Minnis, S.T., Haydock, P.P.J., Ibrahim, S.K., Grove, I.G., Evans, K. and Russell, M.D. (2002) Potato cyst nematodes in England and Wales – occurrence and distribution. Annals of Applied Biology 140, 187–195.

R.P. Blackshaw and B.R. Kerry Mulder, J.G., Diepenhorst, P., Plieger, P. and Bruggemann-Rotgans, E.M. (1992) Hatching agent for the potato cyst nematode. Patent Application PCT/NL92/00 126. Newbold, J.W. (1981) The control of leatherjackets in grassland by winter pesticide applications. Proceedings of Crop Protection in Northern Britain. The Association for Crop Protection in Northern Britain, Dundee, UK, pp. 207–211. Oestergaard, J., Belau, C., Strauch, O., Ester, A., van Rozen, K. and Ehlers, R.U. (2006) Biological control of Tipula paludosa (Diptera: Nematocera) using entomopathogenic nematodes (Steinernema spp.) and Bacillus thuringiensis subsp. israelensis. Biological Control 39, 525–531. Rennie, J. (1916) On the biology and economic significance of Tipula paludosa. Part 1 Mating and oviposition. Annals of Applied Biology 2, 235–240. Riga, E., Perry, R.N., Barrett, J. and Johnston, M.R.L. (1996) Electrophysiological responses of males of the potato cyst nematodes, Globodera rostochiensis and G. pallida, to their sex pheromones. Parasitology 112, 239–246. Seinhorst, J.W. (1965) The relationship between nematode density and damage to plants. Nematologica 11, 137–154. Trudgill, D.L. (1967) Effect of environment on sex determination in Heterodera rostochiensis. Nematologica 13, 263–272. Trudgill, D.L., Evans, K. and Parrott, D.M. (1975) Effects of potato cyst nematodes on potato plants. 1. Effects in a trial with irrigation and fumigation on growth and nitrogen and potassium contents of a resistant and a susceptible variety. Nematologica 21, 169–182. Trudgill, D.L., Evans, K. and Phillips, M.S. (1998) Potato cyst nematodes: damage mechanisms and tolerance in the potato. In: Marks, R.J. and Brodie, B.B. (eds) Potato Cyst Nematodes Biology, Distribution and Control. CAB International, Wallingford, UK, pp. 117–113. Turner, S.J. (1990) The identification and fitness of virulent potato cyst-nematode

Root Herbivory in Agricultural Ecosystems populations (Globodera pallida) selected on resistant Solanum vernei hybrids for up to 11 generations. Annals of Applied Biology 117, 385–397. Turner, S.J. and Evans, K. (1998) The origins, global distribution and biology of potato cyst nematodes (Globodera rostochiensis Woll. and Globodera pallida Stone). In: Marks, R.J. and Brodie, B.B. (eds) Potato Cyst Nematodes: Biology, Distribution and

53 Control. CAB International, Wallingford, UK, pp. 7–26. Urwin, P.E., Troth, K.M., Zubko, E.I. and Atkinson, H.J. (2001) Effective transgenic resistance to Globodera pallida in potato field trials. Molecular Breeding 8, 95–101. Whitehead, A.G. (1995) Decline of potato cyst nematodes, Globodera rostochiensis and Globodera pallida, in spring barley microplots. Plant Pathology 44, 191–195.

4

Root Herbivory in Grassland Ecosystems T.R. SEASTEDT1 AND P.J. MURRAY2 1

The University of Colorado, Boulder, USA; 2North Wyke Research, Devon, UK

4.1. Introduction Temperate grassland systems have a stable and permanent plant cover, which in turn provides a habitat for a large and diverse invertebrate fauna. Curry (1994) estimated that between 70% and 98% of the invertebrate biomass occurs belowground, and this may exceed that of domestic livestock grazing aboveground (Coulson and Butterfield, 1978). In grasslands, between 40% and 60% of net primary production (NPP) occurs belowground (Coleman, 1976). There is a growing body of work which suggests that soil organisms exert an influential role in plant community dynamics (Bever, 2003) and may contribute to plant coexistence. Many of the invertebrates which inhabit the soil of grassland systems are phytophagous and cause insidious losses to plant material belowground. It has been shown that even small populations of phytophagous taxa, acting synchronously, may reduce herbage biomass significantly (Henderson and Clements, 1977) and belowground consumption may be the main fate of primary production in permanent grassland (Bardgett et al., 1999b). Plant–herbivore interactions have been a mainstay of ecological studies for decades, yet relatively little of this research has been focused on studies of root-feeding herbivores (Hunter, 2001; Blossey and Hunt-Joshi, 2003). While earlier studies recognized that foliage herbivory could affect belowground consumers (Stanton et al., 1981; Seastedt, 1985), perhaps the most significant advances in this field in the last decade have involved the recognition and demonstration that the magnitude and consequences of plant–soil herbivore interactions are often mediated by a large number of additional biotic and abiotic variables (Wardle et al., 2004). Among these is the recognition that canopy processes affect soil processes and vice versa (Bardgett and Wardle, 2003; Bezemer et al., 2003). Less well known, and certainly less understood, are the effects and interactions of soil herbivores on other soil inhabitants. 54

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Unlike plant canopies, root herbivores live in intimate contact with a bewildering array of biota, capable of all trophic functions. The process of herbivory therefore often involves concurrent changes in plant–soil-microbe and plant–decomposer organism interactions. For example, the root-feeding leatherjackets (Tipula spp.) have been shown to have a significant impact on communities of soil microbes (Dawson et al., 2004), which may be attributed to changes in root exudation (Treonis et al., 2005). While tissue loss to herbivores has a negative impact on plant fitness, the net effect of the activity must be assessed in terms of responses of all feedbacks to plant growth and reproduction (De Deyn et al., 2004, 2007). In this chapter, we provide a brief overview of the root-feeding herbivore groups that we consider to be most influential in grassland systems. We then attempt an assessment of impacts of these organisms on the productivity of grasslands. Finally, we suggest several approaches to assessing both the direct and indirect effects of root feeders on grasslands and attempt to make some predictions as to how current trends in environmental characteristics (i.e. changes in atmospheric chemistry and plant composition) might affect our assessment of plant–soil herbivore interactions.

4.2. Dominant Root-feeding Herbivores of Grasslands It is difficult to nominate one group of root feeders as the most important herbivores for all grasslands. Nematodes would likely win if soil biologists took such a vote. In North America, nematodes compose the most significant group of herbivores in grasslands (Stanton et al., 1981; Stanton, 1988). This group may occasionally consume as much NPP as do cattle. Nematode densities in soils appear to track root biomass and productivity (Smolik and Lewis, 1982; Freckman and Virginia, 1989; De Deyn et al., 2004), show changes with respect to season and soil moisture (Smolik and Rogers, 1976; Seastedt et al., 1987) and consume perhaps 20–25% of NPP (Stanton et al., 1981; Ingham and Detling, 1986). Porazinska et al. (2003) reported on nematodes associated with grasses at a semi-humid tallgrass prairie site, and found an average of almost 500 plant parasites per 100 g of soil. That report also noted that the highest densities of plant feeders were found on a relatively rare grass species. About 40% of the 357 species of nematodes identified from 48 samples of six grass species were herbivores (Mullin and Powers, 2001). The total densities of nematodes at this site approaches 107 individuals m−2, of which perhaps one-third are herbivores (Todd, 1996). Nematode herbivory appears to be ubiquitous in grasslands. Larger root herbivores, however, seem to show somewhat more restricted distributions. Within North America, New Zealand and Australia, the Scarabeid larvae (white grubs) appear to be important and significant herbivores (Davidson and Roberts, 1969; Ridsdill-Smith, 1977; Hutchinson and King, 1980). However, this group does not appear to be as significant in European grasslands where leatherjackets (Tipulidae) and wireworms (Elateroidea) appear to be the dominant, large arthropod herbivores (Blackshaw, 1984; Jones and

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Jones, 1984; Curry, 1994). Root herbivory by vertebrates is even more localized, but where it occurs its impacts are large (Andersen, 1987). Both vertebrates and the scarab larvae can periodically become locally abundant, thereby having large and often negative effects on target species. In contrast, herbivory by other large insects in North America including cicadas, wire worms and weevils is not known to exhibit ‘outbreaks’, but these species clearly do consume moderate amounts of plant resources (Callaham et al., 2003; Whiles and Charlton, 2006).

4.3. Impacts of Root-feeding Herbivores Root herbivores are known to have many effects on their host plants, for example, they damage and consume plant roots, produce faeces and severed root segments, change the quantity and composition of root exudates and increase root tissue turnover rates (Murray and Clements, 1992; Murray et al., 1996; Dawson et al., 2002). Schädler et al. (2004) demonstrated herbivore effects on plant species composition and succession, a response similar to earlier work by Brown and Gange (1989, 1990, 1992). Sustainable grassland communities (also called late-successional communities) generally experience positive feedbacks from the soil biota that contribute to the persistence of these plant species (Kardol et al., 2006). In developing a general model of herbivore effects in grasslands, current theory indicates that the dominant grass species persist, among other reasons, because they do not experience high rates of density-dependent herbivory, i.e. the density of the host plant does not, in itself, result in unacceptably high rates of herbivory. This does not appear true for early successional species, which appear penalized by the current or previous presence of conspecifics. Belowground herbivory represents one mechanism explaining this phenomenon. Partitioning the various mechanisms responsible for this pattern across multiple grassland types requires an assessment of mutualists, herbivores and pathogens (e.g. Klironomos, 2002; De Deyn et al., 2003). Grasses exhibit a fibrous root morphology, a trait that appears to have large effects on soil characteristics (e.g. Jenny, 1980). Are there potential unique plant–herbivore interactions that result from this growth form? First and foremost, the fine scale of the individual roots suggests that grass root specialists should be small as well. Certainly, the dominance of nematodes as root feeders supports this notion. If invertebrates relegated to the water films within the soil system dominate root feeding, this fact may help explain some important ecological consequences of herbivory. While smaller herbivores are the rule, there remain some very large (from the perspective of the root) herbivores, including the tipulids (Diptera: Tipulidae), white grubs (Coleoptera: Scarabaeidae) and cicadas (Homoptera: Cicadidae). These larger organisms vary in their feeding strategies, with the Homopterans staying largely in place, while the tipulids and scarabs somehow burrow or chew their way from root to root. Scarab larvae can sometimes be found deep (>20 cm) in soils. Their effects on the plant

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system therefore include not only the direct effects of herbivory, but also the potential indirect effects caused by their movements within the root system. The soil disturbance alone is likely to influence soil biota by creating new surface substrates for decomposer organisms.

4.3.1. Herbivore body size and impacts on plant productivity The fact that body size matters in the role of invertebrates in decomposition processes has been known for a long time (e.g. Swift et al., 1979). Macroinvertebrates play potentially larger functions as stimulators of microbial processes than do micro-invertebrates. A similar phenomenon may exist for grass root herbivory. However, here the ‘benefits’ associated with size may be reversed. Simply put, macro-invertebrate root herbivores, in general, appear more likely to have negative effects on their hosts, whereas microherbivores have at least the potential to stimulate compensatory or even overcompensatory growth in their host plants. The response of grass productivity as a result of herbivory is a function of the change (loss) in biomass versus the change (increase, no change or decrease) in relative growth rate of the plant (Hilbert et al., 1981). Hence, herbivory can reduce plant biomass without changing NPP if the increase in growth rate compensates for that biomass loss. Compensatory growth is clearly desirable from both the plant and herbivore perspective: you can have your resource and eat it, too! For foliage herbivores, we know that growth rates occasionally increase faster than biomass loss, resulting in overcompensation and a potential increase in plant fitness (Maschinski and Whitham, 1989; Agrawal, 2000). Only when the percentage of plant biomass increases to a point where increased relative growth rates cannot compensate for this loss does a net loss in plant productivity occur. Some environments do not allow for compensatory growth, so this response is a function of both the herbivores and the available soil resources (Wise and Abrahamson, 2005, 2007; Fig. 4.1). Overcompensation to herbivores feeding on roots has, to our knowledge, not been reported for grasses, but this has been demonstrated for other growth forms (Quinn and Hall, 1992; Thelen et al., 2005). Grasses are known for having a very large percentage of NPP allocated to small roots, and a large percentage of this root biomass is allocated near the soil surface (Jackson et al., 1996). Nematodes, feeding in the water films associated with the rhizosphere, are hypothesized to increase root exudates, microbial growth and, eventually, mineralization processes (Fig. 4.2). As long as root tissue biomass loss is equal to the increase in plant relative growth rate, herbivory produces a compensation effect. In contrast, a macroherbivore, such as a scarab larva, consumes not only the root but the rhizosphere as well. No doubt this includes at least the microflora, if not the micro-invertebrates. Further, relatively low densities of nematodes would remove much less tissue (but still potentially increase root exudation) relative to the ‘first bite’ of an organism the size of many Scarabaeid larvae. Finally, the type of damage is likely to be very different. Cutting a root into

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High

+

Low Micro-herbivores

0

+

a

b

−

0 −

Plant production

Micro-herbivores

Plant production

(B)

(A)

Macro-herbivores Low Low

High Intensity of herbivory

High

Macro-herbivores Numbers of herbivores

Fig. 4.1. Two ways of looking at plant responses to herbivory. Figure 4.1A is a traditional compensation–overcompensation response function (e.g. Seastedt et al., 1988) which suggests that low levels of herbivory by nematodes and other small organisms are more likely to produce a compensatory or overcompensatory response by the plants than that caused by larger herbivores. Due to the nature of herbivory by larger soil animals, small amounts of root consumption may translate into a large amount of root death. In Fig. 4.1B, the x-axis reflects numbers of animals rather than amount of root tissue removed. Here, one scarab larva matches up with hundreds, if not thousands, of plant-feeding nematodes (note that zone ‘a’ does not exist for macro-herbivores). This approach emphasizes that low levels of herbivory by nematodes and other small invertebrates in terms of plant costs are potentially lower than ‘one bite’ from the larger animals. In both figures, the response functions are the same. Small amounts of herbivory (as defined perhaps more by tissue lost to the plant rather than tissue consumed by the herbivore) have the potential to generate overcompensation, but larger amounts tend to have negative effects on the plants.

half, the equivalent of modest herbivory by macro-herbivores in the upper soil horizons results in extensive root death. Punching small holes in the same root could perhaps provide the same amount of material to the herbivores, but the damage to the rooting system would be much less. Thus, herbivore-mediated exchange of plant CHO compounds for enhanced uptake of nitrogen or phosphorus is suggested to be a function of herbivore size. On a weight for weight basis of herbivores, micro-herbivory of roots may have more of a neutral or even beneficial effect than macro-herbivory. To our knowledge, no comparisons of this sort have been done.

4.3.2. Costs of root herbivory in grasslands In grasslands, root herbivores can cause considerable economic losses. However, these are not always evident to the farmer due to the nature of the crop and the way in which it is perceived. In the UK temporary (50% of the carbon captured during photosynthesis (net primary production or NPP) is allocated belowground (Hendrick and Pregitzer, 1992). Although a portion of the carbon that flows down to roots is exuded as ‘rhizodeposition’ (Jaeger et al., 1999) or allocated to symbiotic mycorrhizae (Fogel, 1980), a substantial fraction of the carbon fixed by forests finds its way into root tissue. For example, in sugar maple, Acer saccharum Marshall, forests, the NPP of fine roots can exceed 8000 kg ha−1 year−1, nearly twofold that of foliage NPP (Hendrick and Pregitzer, 1993). Recent estimates of fineroot NPP from a longleaf pine stand in south Georgia, USA, exceed 4600 kg ha−1 year−1 with standing biomass around 1300 kg ha−1 (Hendricks et al., 2006). Although forest biomes vary in the amount of fine-root biomass that they support (Jackson et al., 1997), the numbers are astonishingly large. For example, temperate coniferous forests generate a staggering 6 km of fine-root length per square metre of forest floor (Table 5.1). Whether we notice them or not, forest roots represent a vast potential resource for belowground herbivores. As we might expect, natural selection has driven the evolution of myriad root feeders that can reach extraordinary densities in forests; 3.75 million cicadas ha−1 (Dybas and Davis, 1962), 0.2 million chrysomelids ha−1 (Pokon et al., 2005) and 15 million nematodes m−2 (Sohlenius, 1980). Unfortunately, the ecologies of forest root herbivores, and their impacts upon forest plants 68

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Table 5.1. The abundance of fine roots in major forest biomes of the world. (After Jackson et al., 1997.)

Forest biome Boreal Sclerophyllous Temperate coniferous Temperate deciduous Tropical deciduous Tropical evergreen

Total fine-root biomass (kg m−2)

Live fine-root biomass (kg m−2)

Live fine-root length (km m−2)

0.60 0.52 0.82 0.78 0.57 0.57

0.23 0.28 0.50 0.44 0.28 0.33

2.60 8.40 6.10 5.40 3.50 4.10

Live Percentage fine-root biomass area index in upper (m2 m−2) 30 cm 4.60 11.60 11.00 9.80 6.30 7.40

83 79 45 63 42 57

and ecosystems, are poorly known – the forest is still well hidden beneath the trees. In this chapter, I explore some of the few generalities that appear to be emerging from studies of root herbivores in forests.

5.2. The Architecture of Tree Roots To understand the ecology of root feeders in forests, we need to understand something about forest root systems. The architecture and function of tree roots depend upon several kinds of structure. The largest roots are comprised mainly of perennial woody tissue, and function in phloem and xylem transport, storage of starch and other materials, and structural support. The woody portions of roots are made principally of cellulose and hemicellulose fibres held together by lignin. Only root herbivores that host anaerobic gut symbionts (e.g. termites) can usefully digest woody tissue (Speight et al., 2008). Starch, however, is a relatively energy-rich polysaccharide – a polymer based on glucose used for energy storage by plants. Although lacking in nitrogen, phosphorus and other minerals, it at least provides a ready source of energy for root herbivores that feed on perennial roots. Lateral branches, called fine roots, emerge from perennial roots and are largely responsible for nutrient and water acquisition and the maintenance of mycorrhizae (Pregitzer, 2002). Fine roots also exude organic molecules into the rhizosphere, with apparent effects on local rates of nutrient mineralization and subsequent uptake (Jaeger et al., 1999). The youngest fine roots are non-woody and lack the impermeable suberin (complex organic polymer) layer that controls solute transport within older roots. As such, they are likely nutritionally superior on a per mass basis than older or larger roots. The principal non-structural carbohydrates in fine roots are starch and soluble sugars (Kosola et al., 2002). In many temperate deciduous trees, starch accumulates in roots during the late summer and is used in part to power leaf flush during the following spring. Soluble sugars are presumably used to drive current metabolic activity and to pay the costs of microbial symbioses.

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Because most forest trees host mycorrhizal fungi in their fine roots, all but the smallest root herbivores will necessarily consume fungi as they consume fine roots. Given that mycorrhizal fungi are in the business of gathering phosphorus and nitrogen in return for sugars, we might conclude that mycorrhizae supply nutrients to root herbivores and that fine roots should be a favoured source of food for many root herbivores. From these few basic facts, it is clear that root herbivores have the potential to reduce plant performance in a number of key ways. First, damage to perennial tissues can compromise phloem and xylem transport and the structural integrity of tree support. Second, important reserves for future growth, survival and reproduction can be lost to herbivores. Third, damage to fine roots can reduce the ability of trees to gain nutrients and water, either directly or through their mycorrhizae. Fourth, damage to roots can increase subsequent attack and infection by a broad range of enemies.

5.3. The Importance of Fine Roots Despite being inconspicuous in comparison with perennial roots, fine roots are the key players in plant foraging belowground. Most fine roots are nonwoody and are often categorized rather arbitrarily by size (e.g. 1 mm in diameter. As they pass through each stage and go further from the root tip, fine roots become lower in nitrogen, less metabolically active and likely contribute less to nutrient and water uptake (Hendrick and Pregitzer, 1992; Pregitzer et al., 2002). It is likely that, for many trees, fine roots 90%

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of the French grape-growing regions, which ultimately were replanted with phylloxera-resistant rootstocks of American Vitis parentage. However, this did not stop the insect rapidly spreading to other European grape-growing regions, probably on infested planting material, and later to the continents of Asia, Australasia, Africa and South America.

6.3. Grapevine Phylloxera Research and Management Options 6.3.1. Eradication Eradication of this invasive pest species has been unsuccessful thus far. In most countries where phylloxera is present rootstock replanting has reduced phylloxera abundance and it is seen as the main form of management. In Australia, in the Geelong region of Victoria where phylloxera was first detected in 1877, extensive eradication efforts were made which included destroying all grapevine plantings in the region, about 2000 vineyards in all, by uprooting, burning and soil fumigation with salt or carbon bisulphide (Buchanan, 1990). These attempts ultimately failed and phylloxera moved to other viticulture regions in the states of Victoria and New South Wales. Despite its accidental introduction to Australia in 1875, the geographical distribution of grapevine phylloxera has remained limited to around 2% of the grape-growing regions. It has been detected only in discrete quarantine zones, termed phylloxera-infested zones (PIZs) in Central and North-east Victoria and New South Wales (NVHSC, 2003). However, since the early 1990s there has been a marginal increase in the size of some PIZs and the creation of new quarantine zones due to outbreaks in the King Valley (1991), Upton (2000), Buckland Valley (2003), Yarra Valley (2006) and Macedon (2008) regions of Victoria. Yet, despite these relatively recent detections, Australia remains one of the few grape-growing countries with limited use of phylloxera-resistant rootstocks with 85% of its vineyard area still planted with varieties of the highly susceptible species V. vinifera (Powell et al., 2003), and relatively limited distribution of the pest despite the apparent high risk. Quarantine has clearly played a role in limiting distribution in Australia, but other factors such as soil and climate characteristics may be involved in restricting dispersal and establishment.

6.3.2. Resistant rootstocks The native range of grapevine phylloxera is near the Eastern Rocky Mountains in North America and it would have been restricted to this region until colonization by European settlers who introduced V. vinifera to the area (Granett et al., 2001a). Grapevine phylloxera was inadvertently transferred to Europe on wild American Vitis spp., which were introduced as breeding material to develop hybrids to control the fungal disease powdery mildew. From its early detection in France, breeding programmes focused on the development

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of phylloxera-resistant rootstocks relying on the natural resistance of American Vitis spp. on to which V. vinifera, which possesses quality characteristics important for fruit quality, could be grafted. Resistance to phylloxera is not always the main reason for choosing rootstocks. Nematode resistance, vigour and tolerance to salinity, drought, lime and soil acidity (May, 1994; Dry, 2007) are sometimes more compelling economic reasons to select rootstocks. In Australia, the cost of rootstocks (around fourfold higher than ungrafted grapevines) can be a limitation for some growers. Resistant rootstocks have been highly successful to-date in controlling phylloxera around the world. However, because of this sole reliance on a single form of phylloxera management for >150 years this has limited research into other aspects of phylloxera biology and management.

6.3.3. Genetic diversity and life cycle It has been evident for some time that different phylloxera populations can establish and develop colonies on resistant rootstocks to varying levels of adaptability (Granett et al., 1983) and resistance-breaking biotypes have been reported on rootstock hybrids with partial V. vinifera parentage (Granett et al., 1985), but the genetic variability within phylloxera populations remain poorly understood. The development of improved molecular techniques over the last decade has seen an increased understanding and clarification of the life cycle and genetics of grapevine phylloxera (Corrie et al., 2002, 2003), firstly with the development of random amplification of polymorphic DNA (RAPD) and amplified fragment length polymorphism (AFLP) genetic markers (Fong et al., 1995; Forneck et al., 2000) and more recently with nuclear and mitochondrial DNA markers (Corrie et al., 2002; Vorwerk and Forneck, 2006). The complexity and range of genetic diversity have highlighted the potential for breakdown in phylloxera-resistant rootstocks and the need for selection of rootstocks based on phylloxera genotypic background to reduce the risk of phylloxera transfer. The use of nuclear DNA microsatellite markers has resulted in the characterization and geographical distribution of more than 80 distinct phylloxera genotypes in Australia (Umina et al., 2007). Ecologically distinct clonal lineages are evident and the two most common and widespread lineages termed G1 and G4 (Corrie et al., 2002) are regarded as ‘superclones’ (Umina et al., 2007). Of these known genotypes most are root-feeding (radicicole) only, but others are purely leaf-galling (gallicicole) and relatively few appear to be able to combine both radicicole and gallicicole life habitat (Corrie et al., 2002). In Europe, more than 80 distinct genotypes originating from leaf-galling populations have been identified using microsatellite markers (Vorwerk and Forneck, 2006). Leaf galls, caused by some phylloxera genotypes, generally only occur on American Vitis spp., and there is no evidence that their presence causes any economic impact or yield decline even though they can be quite prolific. Fully protected within the leaf gall, a single female phylloxera

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will develop into the adult stage and asexually produce eggs, which develop into first-instar nymphs that subsequently disperse as the gall opens. A life cycle variant occurs in phylloxera’s native range where it inhabits Vitis leaves only and reproduces by sexual reproduction (Downie, 2000). Differing virulence levels of root-galling genotypes on commercially available rootstocks and ungrafted V. vinifera (Corrie et al., 2003; Viduka et al., 2003; Korosi et al., 2007) have important implications for management of ungrafted vines and selection of phylloxera-resistant rootstocks. When a new outbreak of phylloxera is detected in Australia, insects are now routinely DNA-typed and their population dynamics monitored in the field. This assists the grower in determining both the choice of rootstock and timelines for a replanting programme based on the insect genetics and population biology. DNA typing can also aid in traceback procedures to determine the origin of an infestation (Umina et al., 2007).

6.3.4. Soil environment One important factor which could affect the selection of a rootstock for phylloxera resistance, other than phylloxera genotype, is the virulence of the insect under different soil and climatic conditions. Several studies have examined the effect of temperature on phylloxera development and abundance, reporting that the optimal range for development is between 21°C and 28°C (Granett and Timper, 1987; Fischer and Albrecht, 2003) and gall formation occurs at 18°C (Turley et al., 1996). However, the influence of soil chemical and textural characteristics on phylloxera’s ability to interact and establish on its host and its subsequent rate of dispersal within an infested vineyard has received relatively limited attention. For example, no published studies have examined if root volatiles or exudates are involved in attracting phylloxera to its feeding site and the impact that soil texture may have on any association (see review by Johnson and Gregory, 2006). A Californian study (Nougaret and Lapham, 1928) indicates that sand content is a key factor in phylloxera abundance. A 4-year study under field conditions in Austrian vineyards (Reisenzein et al., 2007) indicated that pH, organic carbon and soil texture influence phylloxera populations. Clay and inorganic content were positively correlated with increased phylloxera abundance, whereas sand and pH had a negative correlation. Survey information from Australian vineyards shows that phylloxera has been detected primarily in clay-loam-based soils (Buchanan, 1990). However, it has also been detected, albeit in lower levels, in soils with relatively high sand content (Powell et al., 2003). Under Australian soil conditions, other factors have been highlighted which may also influence phylloxera abundance and dispersal, including aluminium exchange capacity, which is associated with higher phylloxera abundance when it occurs at toxic levels. The increased phylloxera levels may be attributed to reduced root elongation and restricted water and nutrient uptake, weakening the root system and thus making it more susceptible to phylloxera

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damage (Powell et al., 2003). The rate of spread and establishment of phylloxera has also been linked to higher levels of electrical conductivity in the soil (Bruce et al., 2008), which highlights the potential for soil sensing to be used as part of an integrated targeted phylloxera detection system. The influence of soil characteristics on phylloxera genotype virulence and interactions with root systems could also influence population dynamics on rootstocks. In field observations, the ability of certain genotypes to establish populations on some rootstocks appears to be site-dependent (Trethowan and Powell, 2007) and soil may be a key factor (Powell et al., 2003). Minirhizotron studies (Bauerle et al., 2007) indicate that phylloxera populations on some rootstocks can cause a small decrease in root biomass, but this may not have a significant impact on the roots’ ability to take up water and nutrients. Worldwide current rootstock recommendations do not generally consider phylloxera genetic lineage and/or soil type but utilize rootstock screening of phylloxera ‘populations’ in glasshouse conditions (King et al., 1982), in aseptic tissue culture environments (Grzegorczyk and Walker, 1998; Kellow et al., 2002) or on excised roots (Fergusson-Kolmes and Dennehy, 1993; Kocsis et al., 1999, 2002). Recent research in Australia has focused on the development of a triphasic rootstock screening protocol using single genetic lineages of phylloxera incorporating laboratory, glasshouse and field-based trials (Korosi et al., 2007). However, only limited field studies have been conducted to date to assess rootstock–phylloxera genotype interactions across a range of viticulture sites and these have been restricted to either root survey sampling (Corrie et al., 2003) or emergence trap sampling (Trethowan and Powell, 2007). A range of phylloxera genotypes can establish on commercially available rootstocks under field conditions. Some hybrid rootstocks with some V. vinifera parentage show marked reduction in yield, and quality characteristics differ significantly (Trethowan and Powell, 2007). In general, however, populations appear lower or absent on rootstocks compared to V. vinifera.

6.3.5. Population monitoring The population dynamics of grapevine phylloxera on ungrafted V. vinifera have been studied under commercial field conditions in North America (Omer et al., 1997), Europe (Porten and Huber, 2003) and Australasia (King and Buchanan, 1986; Powell et al., 2003; Herbert et al., 2006). In North America, primarily in California, and Europe, population levels have generally been assessed by destructive and non-destructive assessment of phylloxera and associated damage on the root system of infested grapevines (Granett et al., 2001a; Porten and Huber, 2003). Phylloxera demographics are similar in all regions; populations overwinter on the root systems as first-instar nymphs, which develop to adulthood and reproduce in the spring and reach peak abundance in the summer months; populations decline in autumn. Phylloxera have a high reproductive capability, depending on genetic strain, and each asexual adult can produce several hundred viable eggs.

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A range of trapping systems have been utilized in Australia and New Zealand to monitor the spread rate of phylloxera during the grapevinegrowing season (King and Buchanan, 1986) and assess the potential risk of transfer and provide a scientific basis for quarantine restrictions (Powell et al., 2000). Due to the nature of the insects’ life cycle and habitat, monitoring is conducted both aboveground and belowground. Belowground monitoring of phylloxera is conducted in the form of non-destructive qualitative and quantitative visual assessment of phylloxera on the root system. This system relies on digging around the root zone and quantifying phylloxera and associated root damage in situ or removing root pieces and removing and counting phylloxera life stages. This is a somewhat laborious and time-consuming process and more commonly phylloxera emergence through the soil and subsequent movement aboveground is more readily quantified using collecting devices such as pitfall, sticky or emergence traps (Powell et al., 2000). A number of field studies have been conducted on the population dynamics of individual phylloxera genotypes on ungrafted V. vinifera in different grapegrowing regions of Australia (Herbert et al., 2006; Powell et al., 2007b). The development, more recently, of a phylloxera-specific DNA probe which can detect and quantify phylloxera DNA in soil samples has improved the accuracy of determining population levels in a range of soil conditions and areas, where abundance levels may be below the limits of trap detection (Herbert et al., 2007). Unlike other screening techniques, a DNA probe could be potentially used at any time of the year and be modified to provide information on the genetic identity of the phylloxera.

6.3.6. Feeding physiology and anatomy Phylloxera are obligate biotrophs, which feed only on Vitis spp. Radicicole phylloxera feed on susceptible Vitis roots causing the initiation of a gall. The type of gall development is dependent on the root lignification status. Nonlignified immature or feeder roots develop root galls, which appear as yellow fleshy hook-like structures called nodosities (Fig. 6.1B). Nodosities can appear in masses on the root system or be relatively small or indistinct depending on the genotype of both host and pest. Nodosities can develop on both ‘resistant’ Vitis spp. and ungrafted susceptible V. vinifera. On mature lignified roots tuberosities (Fig. 6.1C) develop on lignified roots of V. vinifera only and this species appears to have either no or limited defence response. Tuberosities are localized root swellings, which may become crater-like in appearance and necrotic, acting as a potential entry site of opportunistic fungal pathogens. The level of damage in vineyards is therefore likely to be closely related not only to the phylloxera virulence level, but also to the diversity and level of microbial activity (Edwards et al., 2006a). Histological studies of root-feeding phylloxera indicate that on V. vinifera the insect feeds on single parenchymal cells in the outer region of the cortex, as evidenced by single stylet tracks left behind after stylet withdrawal (Kellow et al., 2004), whereas when feeding on ‘resistant’ rootstocks stylet

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tracks are multiple and branching, indicating repeated stylet-probing activity. Sucrose and amino acids gradually accumulate in the nodosities initiated by feeding, which then act as a nutrient sink for the insect allowing it to develop to maturity and reproduce (Fig. 6.1D). Artificial diet studies conducted on both leaf-galling (Forneck and Wöhrle, 2003) and root-galling phylloxera (Kingston et al., 2007) indicated that phylloxera require sucrose and amino acids in their diet and an acidic pH for development, but other chemical components are required for optimal development. Physiological studies on phylloxera have highlighted that the internal morphology of the digestive system is atypical and differs from phloemfeeding Hemiptera in that it has a compartmentalized midgut with the posterior region having a storage role prior to digestion activities in the anterior region (Kingston et al., 2007). This may aid the insect in producing enough nutritional reserves to survive for up to 1 week away from its host plant and as an energy source for egg production (Kingston et al., 2007). The role of endosymbionts, in the form of bacteria, does not appear to be an obligate endosymbiosis, but more a transient relationship (Kingston, 2007; Vorwerk et al., 2007). This requires further investigation as symbionts may be involved in the insects’ virulence and adaptability to different Vitis hosts and could therefore be important when assessing host plant–insect interactions with rootstocks. Electrophysiological studies using a system called electrical penetration graph (EPG) (Tjallinge, 1988) have been widely used to study the feeding behaviour of a range of fluid-feeding insects. This system was recently adapted for the first time to characterize feeding behaviour of root-feeding grape phylloxera on susceptible and resistant roots (Kingston, 2007). Further development of this approach could lead to an improved understanding of the mechanisms of resistance to grapevine phylloxera and improve rootstock screening approaches to specific phylloxera genotypes.

6.3.7. Fungal interactions In addition to the physiological response of the grapevine to phylloxera activity on its root system, the feeding site itself creates entry points for fungal pathogens within the soil. A close association between grapevine phylloxera presence and soil-borne fungal infection of roots has been observed. Fusarium spp., Cylindrocarpon destructans and Phaeoacremonium spp. cause more severe damage when in the presence of phylloxera, both under controlled conditions and in phylloxera-infested vineyards (Granett et al., 1998; Edwards et al., 2006b). Under laboratory conditions, inoculations with pathogenic fungi at phylloxera-feeding sites induced root rotting within 6 weeks (Omer, 2000). The presence of fungal pathogens in the roots of phylloxera-infested grapevines could impact not only on the rate and extent of grapevine decline, but also on the efficacy of novel chemical and spectral detection methods currently under development (Renzullo et al., 2004; Blanchfield et al., 2006), as the presence of fungi may change the stress or defence signal produced in infested vines.

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6.3.8. Cultural management Although there have been some reports of potential breakdown in rootstock resistance to phylloxera in Europe (Porten et al., 2000) and the USA (Granett et al., 2001b) these are limited. However, interim or alternative management options for phylloxera require some consideration. Cultural options which have been examined include the potential use of soil mulches. Mulch application can change the physical and textural properties of the soil environment, making it either more or less conducive to phylloxera feeding on the root system or directly affecting the insects’ mobility through the soil. Moisture content and temperature of the soil could also vary under differing soil management conditions. Phylloxera development is directly affected by vine physiology (Omer et al., 2002) and moisture and temperature changes in the environment (Granett and Timper, 1987). The chemical composition of a mulch formulation is likely to impact on grapevine physiological response and hence phylloxera–grapevine interactions. Limited studies have been conducted to date, but green waste compost application as a mulch has been shown to increase the risk of phylloxera dispersal aboveground (Powell et al., 2007b), whereas some sawdust and composted grape marc or pomace-based formulations reduce phylloxera abundance (Porten et al., 2000; Huber et al., 2003; Powell et al., 2007d) aboveground and belowground.

6.3.9. Biological control Biological control for grapevine phylloxera has received surprisingly little attention despite the insect being an exotic pest. Entomopathogenic nematodes have been tested under laboratory conditions, but with only limited success (English-Loeb et al., 1999). Some pilot studies have been conducted using microbial agents, such as Beauveria bassiana (Balsamo) Vuillemin (Granett et al., 2001b) and Metarhizium anisopliae (Metschn.) Sorokïn (Kirchmair et al., 2004). While both microbial agents showed good control in vitro, only M. anisopliae has been tested and proven successful in field application (Huber and Kirchmair, 2007). Even so, establishment rates, registration requirements, benefit/cost ratios, soil conditions and nontarget effects need to be fully evaluated before this agent could be used commercially. There are also many natural generalist invertebrate predators in the vineyard ecosystem, both aboveground and belowground, which could be potentially considered as part of an integrated pest management (IPM) programme. In some regions where phylloxera remain quite limited in their distribution the potential for a classical biological control approach remains promising and further research in this field is warranted, but this has rarely been considered despite natural enemies being present in its native habitat. Manipulating the host plant resistance through genetic modification may also be a future management option. Although studies in this area are limited

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for phylloxera, secondary metabolites, such as cyanogenic glucosides, when expressed in V. vinifera roots affect phylloxera fecundity under laboratory conditions (Franks et al., 2006).

6.3.10. Chemical control The search to find a chemical insecticide that is effective against grapevine phylloxera remains elusive and has been ongoing since the early attempts in 19th-century France (Campbell, 2004). Several factors make the control of root-galling grapevine phylloxera difficult using chemical insecticides. The insects’ life cycle and distribution, and chemical residues in grapes, are the major factors to consider. Phylloxera can be found on grapevine roots several metres deep into the soil profile (De Klerk, 1972; Buchanan, 1990) and root distribution is dependent on soil and grapevine type. Depending on the level of infestation and spatial distribution (which is difficult to assess without extensive ground surveying) soil drenches, if they were to be effective, would need to be used at uneconomical and environmentally unfriendly levels. The danger of non-target effects should also be considered. In many countries, maximal residue levels and label restrictions would limit applications of some pesticides. Several phylloxera generations per season can overlap; therefore, optimal timing and repeated application would be critical. Drip irrigation, which in some countries is a preferred method of insecticide delivery, would not give sufficient coverage of the root system as much of the root system is distributed outside the drip zone. Because phylloxera is predominantly a root feeder, downwardly mobile systemic action is important for targeted delivery of the insecticide. The neonicotinoids are downwardly mobile systemics which have a high residual activity and are effective against a broad range of sap-sucking insects. In a recent Australian study (Herbert et al., 2008a), two neonicotinoids, imidacloprid (Bayer Crop Science) and thiamethoxam (Syngenta), were shown to be effective both in vitro and in planta under controlled environment studies. However, their efficacy under field conditions, particularly on clay-loam soils where phylloxera persists, has yet to be proven and consequently there are no registered chemical insecticides for phylloxera control in Australia. Imidacloprid also has an extremely long half-life in the soil, up to 365 days, a high water solubility and is toxic to common predators in vineyards such as the brown lacewing Micromus tasmaniae (Walker) (Neuroptera: Hemerobiidae) (Bernard et al., 2007) and predatory bugs. Thiamethoxam can also be toxic to beneficial predators. Any use of either of these chemicals would need to consider carefully the potential impact on the natural ecosystem.

6.3.11. Quarantine measures Of all the phylloxera life stages, the two actively dispersive forms are the alates (winged adults) and the first-instar nymphs (crawlers), which move

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both aboveground and belowground. Alates are considered of lower risk particularly under Australian and European conditions, as evidence for the sexual component of the life cycle is limited (Corrie et al., 2002; Vorwerk and Forneck, 2006) and their relative abundance in comparison with crawlers is low (Powell et al., 2000). However, crawlers predominate throughout the season belowground on the root system. In spring and summer, due to increasing soil temperatures (Granett and Timper, 1987), crawlers emerge from the soil, sometimes in extremely high numbers (Herbert et al., 2006) and can disperse on to the grapevine foliage and grape bunches (Powell et al., 2000). Because crawlers cannot move more than 100 m in a season by natural dispersal (King and Buchanan, 1986), their spread by human-assisted vectors and subsequent impact on the industry can be effectively controlled through the use of effective and enforced quarantine regulations. Unfortunately, in most grape-growing countries quarantine regulations are either difficult to enforce, such as in Europe with more open cross-border movement, or unmanageable because of an unwillingness to accept market restrictions in movement of grape products and viticultural machinery by the industry as a whole. Others may consider the use of rootstocks alone as sufficient protective measure. However, Australia provides a classic (and perhaps unique) example of how quarantine can play a major role in restricting the spread of a potentially economically devastating but relatively slow-moving insect pest. Phylloxera quarantine boundaries and protocols have been established historically to restrict its spread and remain in place today (Buchanan, 1990). Currently, whenever a ‘new’ phylloxera detection occurs in Australia, if it is outside an existing PIZ, an immediate quarantine is enforced with a minimum boundary of 5 km from the infested vineyard to restrict its spread and quarantine regulations are enforced. While there have been sporadic outbreaks of phylloxera in Victoria and New South Wales, phylloxera distribution is currently restricted to around 2% of grapevine plantings despite the fact that 85% of the grapevines planted in Australia are the susceptible species V. vinifera. Because natural dispersal is so limited the major risks of transfer are on infested material including viticulture machinery, clothing and footwear; planting material; soil; and certain grape products. The presence of crawlers on grapes at vintage (Powell et al., 2000) means they could be inadvertently transferred from an infested vineyard either to a winery in grape bins or to an uninfested vineyard on mechanical grape harvesters, or the clothing or footwear of grape pickers, if quarantine precautions are not adhered to. Other major sources of phylloxera movement are planting material and soil. Phylloxera can be potentially transported on grapevine planting material as rootlings or potted vines, which can harbour all phylloxera life stages and represent a significant risk. Even postharvest grape material such as grapes or unfermented pomace (a mixture of grape seeds, skins and stalks), and other winery waste products are considered a risk as they can carry viable phylloxera crawlers (Deretic et al., 2003; Korosi et al., 2008). Phylloxera cannot survive postharvest fermentation (Deretic et al., 2003), sulphur dioxide fumigation (Buchanan, 1990) or composting (Bishop et al., 2002), but can

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survive for several days submerged in water (Korosi et al., 2008). For these reasons detailed National Quarantine Management Protocols have been developed in Australia to reduce the risk of movement of potential phylloxera-infested material from infested to uninfested regions (NVHSC, 2003). These protocols, along with historical geographic isolation of vineyard regions and creation of quarantine zones, may partially explain why the distribution of phylloxera in Australia is limited, although soil conditions and phylloxera genotype virulence could also be restricting establishment (Powell et al., 2003). Few other countries operate this same high level of quarantine which considers such a broad range of quarantine risks including people, machinery, plant material and soil. In neighbouring New Zealand, where phylloxera was first detected in 1885, it is found in all major grape-growing regions. There are two basic disinfestation approaches used to ameliorate some risks of phylloxera transfer based on phylloxera’s sensitivity to high temperature, low humidity and chemicals. Heat treatment is used in the form of hot-water treatment of vine cuttings (used as planting material) and grape bins and as dry heat treatment for machinery and soil (NVHSC, 2003; Korosi et al., 2008). Chemical treatment in the form of 2% (active ingredient) sodium hypochlorite is routinely used for the disinfestation of footwear, worn by vineyard workers or visitors, and hand implements (Dunstone et al., 2003). As phylloxera has been shown to survive for up to 8 days in the absence of a food source (Kingston et al., 2007) preventing the risk of transfer is ultimately down to the effectiveness of, and adherence to, quarantine protocols, and complacency can result in substantial financial losses for the individual grapegrower and result in market access restrictions for growers in PIZs.

6.3.12. Detection and surveillance The first stage in any phylloxera management programme is to detect the insect, which is a challenge in itself due to its small size and spatial distribution, and a range of detection options are being explored (Herbert et al., 2003; Renzullo et al., 2004; Powell et al., 2007c). Phylloxera in its most dispersive stage, the first instar, is relatively small (0.3 mm in length) and hence not easily visible to the naked eye. The root-galling form spends most of its life as belowground phylloxera feeding on the grapevine root system. It can be present in high abundance or in relatively low numbers depending on its genetic identity and its host plant genotype. Generally, the first indication that phylloxera may be present in a vineyard is seen when grapevines show stress symptoms in the foliage or canopy. This can be expressed as premature senescence in autumn, stunting of lateral shoot growth, reduced grape yields, reduced overall vigour or a general weak spot within a group of vines. However, once a weak spot is detected phylloxera has been present for several years and is highly likely to have spread to other vines, which appear relatively vigorous (Herbert et al., 2003).

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6.3.13. Chemical fingerprinting The possibility of detecting phylloxera presence on grapevine roots by identifying a ‘phylloxera-specific’ chemical marker or markers induced in the leaves or grapes has recently been examined using nuclear magnetic resonance (NMR), mass spectroscopy and high-performance liquid chromatography (HPLC). Principal component analysis of 1H NMR spectra of field- and glasshouse-grown leaves has been conducted and preliminary studies do tentatively indicate that the leaves and roots of phylloxera-infested grapevines express different metabolites and different ratios of metabolites and therefore potential ‘infestation’ markers (Tucker et al., 2007) compared to uninfested grapevine leaves; but the effect could be transient. Ultimately, this approach needs to be validated under a range of conditions including using different grapevine varieties, grafted grapevines, under different edaphic conditions and on grapevines exposed to other stresses (e.g. water, nutrients) to determine whether any marker compounds detected are truly specific to phylloxera infestation rather than general indicators of stress and to optimize timing of detection based on vine phenology.

6.3.14. Spectral fingerprinting The advent of precision viticulture (Proffitt et al., 2006), and in particular the use of remote-sensing devices such as spectral sensors for measuring canopy reflectance and electromagnetic induction sensors to map soil and crop variability across vineyards and grape-growing regions, has improved management and profitability of viticulture industries worldwide. An advantage of remote-sensing technology, which is being explored, is its potential application for pest detection, surveillance and improved management on an area-wide basis. Multispectral sensors can be used remotely, via satellite or aircraft, or on ground-based equipment. These sensors measure canopy reflectance in the solar reflective region of the electromagnetic spectrum covering 4–6 bands. Their potential for use as detection tools focusing on weak spot sites for targeted ground surveys for phylloxera infestation has been explored in North America and Australia (Johnson et al., 1996; Lobitz et al., 1997; Renzullo et al., 2004). They can also prove useful in monitoring temporal and spatial change in phylloxera distribution in known infested vineyards (Frazier et al., 2004). Phylloxera feeding activity on the root system, and its gradual destruction, causes gradual decline in the grapevine canopy quality and area of ungrafted V. vinifera as the vine’s ability to transport water and nutrients is impaired due to damaged root systems. The canopy decline initially shows up as a weak spot, which gradually spreads like an oil spot and satellite spots may appear through an infested vineyard. Initially colour infrared photography was used to detect areas of decreased vegetative growth in the grapevine canopy (Wildman et al., 1983). Then, with the use of improved digital imagery and sensors such as the Compact Airborne Spectrographic Imager (CASI), imagery could be evaluated and manipulated

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in more detail (Johnson et al., 1996). Most of the focus for detection has been on the near-infrared (760–1600 nm) and red (650–700 nm) regions of the reflectance spectra. The mechanism behind this is closely related to the photosynthetic activity of the canopy. The pre-visual signs of grapevine stress in the leaves, due to phylloxera presence on the roots, are associated with a reduction in leaf chlorophyll (Baldy et al., 1996) and an increase in photoprotective pigments (Blanchfield et al., 2006). Although this approach offers potential for an area-wide surveillance for phylloxera (Edwards, 2003) multispectral sensors in effect can only highlight general reductions in canopy vigour; which could be caused by other stresses caused by nutrient and water deficiencies or other pests and diseases. In addition, multispectral imagery would not be suitable for the detection of low virulent phylloxera genotypes or for use in areas of phylloxera-tolerant rootstock plantings, where reduced grapevine vigour may be either delayed or completely absent. Because of the difficulties in distinguishing phylloxera ‘weak’ spots from weak spots caused by other site-related factors, hyperspectral imaging has been developed and tested under both controlled environment and field conditions for phylloxera-specific spectral signatures using hand-held spectrometers (Renzullo et al., 2004). Hyperspectral sensors take 1 nm interval measurements between the 400 and 2500 nm reflective range and have therefore increased sensitivity compared to multispectral sensors. Post-processing of hyperspectral data acquired, using statistical discriminant analysis, is required to find narrow spectral features that may be exploited to separate phylloxera infestation from other stresses (Renzullo et al., 2006b). Findings at least at the leaf level show that the method can separate phylloxera-infested vines from vines subjected to other stresses such as water and nitrogen deficiency even over a 9-week period. The most obvious differences in leaf reflectance spectra occur in the green peak (500–600 nm) and chlorophyll well (550–700 nm) regions, which are closely related to chlorophyll content (Renzullo et al., 2006a). However, further validation, particularly at the canopy scale, is required as separation of phylloxera-specific spectral characteristics can be confused by differences in vine phenology, period since infestation, phylloxera genotype virulence level, soil conditions, canopy management and vine variety. Integration of other field-collected data such as spatial soil maps, phylloxera abundance data and soil classification could, in the future, improve the sensitivity of remote canopy imaging systems (Powell et al., 2007a).

6.3.15. Molecular fingerprinting One of the most recent advances in phylloxera detection is the use of a phylloxera-specific DNA probe. This has been validated under laboratory (Herbert et al., 2007) and field conditions (Herbert et al., 2008b). Under field conditions, the approach appears more sensitive compared with conventional ground surveying and trapping in ungrafted V. vinifera vineyards.

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Unlike other detection techniques, the method could also potentially be used all year round. However, this does require further validation under a range of soil conditions in the field.

6.4. Conclusion Although the selection of phylloxera-resistant rootstocks has been seen as the only long-term solution to phylloxera management, reliance on a single option has to a large extent restricted the research activities conducted on phylloxera for well over a century. Improved technologies in the molecular, physiological, imaging and remote-sensing areas have seen a renewed interest in phylloxera research, particularly in the areas of detection and rootstock management based on phylloxera genetics. Yet despite the fact that phylloxera is predominantly a soil-borne pest, attacking the root system of its host, knowledge of its ecology and the tritrophic interactions between the insect, the host plant and the soil environment have received little attention. Grapevine phylloxera is likely to remain a problem, and potentially a worse problem if climate change impacts on its distribution and host–plant interactions, for the viticulture industry worldwide if these fundamental issues are not addressed.

References Baldy, R., De Benedictis, J., Johnson, L., Weber, E., Baldy, M., Osborn, B. and Burleigh, J. (1996) Leaf color and vine size are related to yield in a phylloxera-infested vineyard. Vitis 35, 201–205. Bauerle, T.L., Eissenstat, D.M., Granett, J., Gardner, D.M. and Smart, D.R. (2007) Consequences of insect herbivory on grape fine root systems with different growth rates. Plant, Cell and Environment 30, 786–795. Bernard, M., Horne, P.A., Papacek, D., Jacometti, M.A., Wratten, S.J., Evans, K.J., Herbert, K.S., Powell, K.S., Rakimov, A., Weppler, R., Kourmouzis, T. and Yen, A.L. (2007) Guidelines for environmentally sustainable wine grape production in Australia: IPM adoption self-assessment guide for growers. Australian and New Zealand Grapegrower and Winemaker 518, 26–36. Bishop, A.L., Powell, K.S., Gibson, T.S., Barchia, I.M. and Wong, P.T.W. (2002)

Mortality of grape phylloxera in composting organics. Australian Journal of Grape and Wine Research 8, 48–55. Blackman, R.L. and Eastop, V.E. (1994) Aphids on the World’s Trees, 1st edn. CAB International, Wallingford, UK. Blanchfield, A.L., Robinson, S.A., Renzullo, L.J. and Powell, K.S. (2006) Phylloxerainfested grapevines have reduced chlorophyll and increased photoprotective pigment content – can leaf pigment composition aid pest detection? Functional Plant Biology 33, 507–514. Bruce, R.J., Mackie, A.M., Korosi, G.A., Lamb, D.W. and Powell, K.S. (2008) Targeted surveillance approach for detection of grapevine phylloxera Daktulosphaira vitifoliae Fitch. Acta Horticulturae (in press). Buchanan, G.A. (1990) The distribution, biology and control of grape phylloxera, Daktulosphaira vitifoliae (Fitch), in Victoria. PhD thesis. La Trobe University, Melbourne, Australia.

Grape Phylloxera Campbell, C. (2004) Phylloxera: How Wine Was Saved for the World, 1st edn. HarperCollins, London. Corrie, A.M., Crozier, R.H., Van Heeswijck, R. and Hoffmann, A.A. (2002) Clonal reproduction and population genetic structure of grape phylloxera, Daktulosphaira vitifoliae, in Australia. Heredity 88, 203–211. Corrie, A.M., van Heeswijck, R. and Hoffmann, A.A. (2003) Evidence for host-associated clones of grape phylloxera Daktulosphaira vitifoliae (Hemiptera: Phylloxeridae) in Australia. Bulletin of Entomological Research 93, 193–201. De Klerk, C.A. (1972) Occurrence and distribution of the vine phylloxera, Phylloxera vitifolia (Fitch), in the Olifants River Irrigation Area, Northwest Cape Province. Phytophylactica 4, 25–26. Deretic, J., Powell, K.S. and Hetherington, S.L. (2003) Assessing the risk of phylloxera transfer during post-harvest handling of wine grapes. Acta Horticulturae 617, 61–66. Downie, D.A. (2000) Patterns of genetic variation in native grape phylloxera on two sympatric host species. Molecular Ecology 9, 505–514. Dry, N. (2007) Grapevine Rootstocks: Selection and Management for South Australian Vineyards. Lythrum Press, Adelaide, Australia. Dunstone, R.J., Corrie, A.M. and Powell, K.S. (2003) Effect of sodium hypochlorite on first instar phylloxera (Daktulosphaira vitifoliae Fitch) mortality. Australian Journal of Grape and Wine Research 9, 107–109. Edwards, E.J., McCaffery, S. and Evans, J.R. (2006a) Phosphorus availability and elevated CO2 affect biological nitrogen fixation and nutrient fluxes in a clover-dominated sward. New Phytologist 169, 157–167. Edwards, J., Powell, K.S. and Granett, J. (2006b) Tritrophic interactions between grapevines, phylloxera and pathogenic fungi – establishing the root cause of grapevine decline. Australian and New Zealand Grapegrower and Winemaker 513, 33–37. Edwards, J. (2003) Identification of phylloxera, the grapevine pest, using high resolution infrared aerial imagery. MSc thesis. Adelaide University, Adelaide, Australia.

111 English-Loeb, G., Villani, M., Martinson, T., Forsline, A. and Consolie, N. (1999) Use of entomopathogenic nematodes for control of grape phylloxera (Homoptera: Phylloxeridae): a laboratory evaluation. Environmental Entomology 28, 890–894. EPPO (1990) Data Sheets on Quarantine Pests Viteus vitifoliae (European and Mediterranean Plant Protection Organisation). CAB International, Wallingford, UK. Fergusson-Kolmes, L.A. and Dennehy, T.J. (1993) Differences in host utilization by populations of North American grape phylloxera (Homoptera, Phylloxeridae). Journal of Economic Entomology 86, 1502–1511. Fischer, J.R. and Albrecht, M.A. (2003) Constant temperature life tables of populations of grape phylloxera from Washington and Oregon. Acta Horticulturae 617, 43–48. Fong, G., Walker, M.A. and Granett, J. (1995) RAPD assessment of California phylloxera diversity. Molecular Ecology 4, 459–464. Forneck, A. and Wöhrle, A. (2003) A synthetic diet for phylloxera (Daktulosphaira vitifoliae Fitch). Acta Horticulturae 617, 129–134. Forneck, A., Walker, M.A. and Blaich, R. (2000) Genetic structure of an introduced pest, grape phylloxera (Daktulosphaira vitifoliae Fitch), in Europe. Genome 43, 669–678. Forneck, A., Kleinmann, S., Blaich, R. and Anvari, S.F. (2002) Histochemistry and anatomy of phylloxera (Daktulosphaira vitifoliae) nodosities on young roots of grapevine (Vitis spp.). Vitis 41, 93–97. Franks, T.K., Powell, K.S., Choimes, S., Marsh, E., Iocco, P., Sinclair, B.J., Ford, C.M. and van Heeswijck, R. (2006) Consequences of transferring three sorghum genes for secondary metabolite (cyanogenic glucoside) biosynthesis to grapevine hairy roots. Transgenic Research 15, 181–195. Frazier, P., Whiting, J., Powell, K.S. and Lamb, D. (2004) Characterising the development of grape phylloxera infestation with multitemporal near-infrared aerial photography. Australian and New Zealand Grapegrower and Winemaker 485, 133–142. Granett, J. and Timper, P. (1987) Demography of grape phylloxera, Daktulosphaira vitifo-

112 liae (Homoptera, Phylloxeridae), at different temperatures. Journal of Economic Entomology 80, 327–329. Granett, J., Bisabriershadi, B. and Carey, J. (1983) Life-tables of phylloxera on resistant and susceptible grape rootstocks. Entomologia Experimentalis et Applicata 34, 13–19. Granett, J., Timper, P. and Lider, L.A. (1985) Grape phylloxera (Daktulosphaira vitifoliae) (Homoptera, Phylloxeridae) biotypes in California. Journal of Economic Entomology 78, 1463–1467. Granett, J., Omer, A.D., Pessereau, P. and Walker, M.A. (1998) Fungal infections of grapevine roots in phylloxera-infested vineyards. Vitis 37, 39–42. Granett, J., Omer, A.D. and Walker, M.A. (2001a) Seasonal capacity of attached and detached vineyard roots to support grape phylloxera (Homoptera: Phylloxeridae). Journal of Economic Entomology 94, 138–144. Granett, J., Walker, M.A., Kocsis, L. and Omer, A.D. (2001b) Biology and management of grape phylloxera. Annual Review of Entomology 46, 387–412. Grzegorczyk, W. and Walker, M.A. (1998) Evaluating resistance to grape phylloxera in Vitis species with an in vitro dual culture assay. American Journal of Enology and Viticulture 49, 17–22. Herbert, K.S., Powell, K.S., Hoffmann, A.A., Parsons, Y., Ophel-Keller, K. and Van Heeswijck, R. (2003) Early detection of phylloxera – present and future directions. Australian and New Zealand Grapegrower and Winemaker 473, 93–96. Herbert, K.S., Hoffmann, A.A. and Powell, K.S. (2006) Changes in grape phylloxera abundance in ungrafted vineyards. Journal of Economic Entomology 99, 1774–1783. Herbert, K.S., Ophel-Keller, K., McKay, A., Powell, K.S. and Hoffmann, A.A. (2007) Towards a routine DNA test for grape phylloxera. Australian and New Zealand Grapegrower and Winemaker 30–33. Herbert, K.S., Hoffmann, A.A. and Powell, K.S. (2008a) Assaying the potential benefits of thiamethoxam and imidacloprid for phylloxera suppression and improvements to grapevine vigour. Crop Protection 27, 1229–1236.

K.S. Powell Herbert, K.S., Powell, K.S., Ophel-Keller, K., McKay, A., Hartley, D., Herdina, Schiffer, M. and Hoffmann, A.A. (2008b) A diagnostic probe for grape phylloxera applicable to soil samples. Journal of Economic Entomology 101, 1–10. Hill, D.S. (1994) Agricultural Entomology, 1st edn. Timber Press, Portland, Oregon. Huber, L. and Kirchmair, M. (2007) Evaluation of efficacy of entomopathogenic fungi against small-scale grapedamaging insects in soil: experiences with grape phylloxera. Acta Horticulturae 633, 167–171. Huber, L., Eisenbeis, G., Porten, M. and Ruhl, E.H. (2003) The influence of organically managed vineyard soils on the phylloxera populations and the vigour of grapevines. Acta Horticulturae 617, 55–59. Johnson, L., Lobitz, B., Armstrong, R., Baldy, R., Weber, E., De Benedictus, J. and Bosch, D. (1996) Airborne imaging aids vineyard canopy evaluation. California Agriculture 50, 14–18. Johnson, S.N. and Gregory, P.J. (2006) Chemically-mediated host–plant location and selection by root-feeding insects. Physiological Entomology 31, 1–13. Kellow, A.V., McDonald, G., Corrie, A.M. and Van Heeswijck, R. (2002) In vitro assessment of grapevine resistance to two populations of phylloxera from Australian vineyards. Australian and New Zealand Grapegrower and Winemaker 8, 109–116. Kellow, A.V., Sedgley, M. and Van Heeswijck, R. (2004) Interaction between Vitis vinifera and grape phylloxera: changes in root tissue during nodosity formation. Annals of Botany 93, 581–590. King, P.D. and Buchanan, G.A. (1986) The dispersal of phylloxera crawlers and spread of phylloxera infestations in New Zealand and Australian vineyards. American Journal of Enology and Viticulture 37, 26–33. King, P.D., Meekings, J.S. and Smith, S.M. (1982) Studies of the resistance of grapes (Vitis spp.) to phylloxera (Daktulosphaira vitifoliae).New Zealand Journal of Experimental Agriculture 10, 337–344. Kingston, K.B. (2007) Digestive and feeding physiology of grape phylloxera (Daktulo-

Grape Phylloxera sphaira vitifoliae Fitch). PhD thesis. Australian National University, Canberra, Australia. Kingston, K.B., Powell, K.S. and Cooper, P.D. (2007) Grape phylloxera: new investigations into the biology of an old grapevine pest.Australian and New Zealand Grapegrower and Winemaker 521, 12–17. Kirchmair, M., Huber, L., Porten, M., Rainer, J. and Strasser, H. (2004) Metarhizium anisopliae, a potential agent for the control of grape phylloxera. Biocontrol 49, 295–303. Kocsis, L., Granett, J., Walker, M.A., Lin, H. and Omer, A.D. (1999) Grape phylloxera populations adapted to Vitis berlandieri × V. riparia rootstocks. American Journal of Enology and Viticulture 50, 101–106. Kocsis, L., Granett, J. and Walker, M.A. (2002) Performance of Hungarian phylloxera strains on Vitis riparia rootstocks. Journal of Applied Entomology – Zeitschrift für Angewandte Entomologie 126, 567–571. Korosi, G.A., Trethowan, C.J. and Powell, K.S. (2007) Screening for rootstock resistance to grapevine phylloxera genotypes from Australian vineyards under controlled conditions. Acta Horticulturae 733, 159–166. Korosi, G.A., Trethowan, C.J. and Powell, K.S. (2008) Reducing the risk of phylloxera transfer on viticultural waste and machinery. Acta Horticulturae (in press). Lobitz, B., Johnson, L., Armstrong, R., Hlvaka, C. and Bell, C. (1997) Grapevine remote sensing analysis of phylloxera early stress (GRAPES): Remote sensing analysis summary. NASA Technical Memo 112218, California, USA. May, P. (1994) Using Grapevine Rootstocks: The Australian Perspective, 1st edn. Winetitles, Adelaide, Australia. Nougaret, R.L. and Lapham, M.H. (1928) A study of phylloxera infestation in California as related to types of soils. USDA Technical Bulletin 20, 1–39. NVHSC (2003) National phylloxera management protocols (National Vine Health Steering Committee). Available at: http:// www.gwrdc.com.au/nvhscphylloxera.htm. OIV (2007) Statistiques Vitivinicoles Mondiales. Organisation Internationale de la Vigne et du Vin, Paris, France.

113 Omer, A.D. (2000) Interaction between grape phylloxera and fungal infections of grapevine roots. In: Powell, K.S. and Whiting, J. (eds) Proceedings of the International Symposium on Grapevine Phylloxera Management. Department of Natural Resources and Environment, Melbourne, Australia, pp. 51–56. Omer, A.D., Granett, J., De Benedictis, J.A. and Walker, M.A. (1995) Effects of fungal root infections on the vigor of grapevines infested by root-feeding grape phylloxera. Vitis 34, 165–170. Omer, A.D., Granett, J., Downie, D.A. and Walker, M.A. (1997) Population dynamics of grape phylloxera in California vineyards. Vitis 36, 199–205. Omer, A.D., Granett, J. and Walker, M.A. (2002) Influence of plant growth stage on grape phylloxera (Homoptera: Phylloxeridae) populations. Environmental Entomology 31, 120–126. Ordish, G. (1972) The Great Wine Blight, 1st edn. Sidgewick & Jackson, London. Porten, M. and Huber, L. (2003) An assessment method for the quantification of Daktulosphaira vitifoliae (Fitch) (Hem., Phylloxeridae) populations in the field. Journal of Applied Entomology – Zeitschrift für Angewandte Entomologie 127, 157–162. Porten, M., Schmid, J. and Ruhl, E.H. (2000) Current problems with phylloxera on grafted vineyards in Germany and ways to fight them. In: Powell, K.S. and Whiting, J. (eds) Proceedings of the International Symposium on Grapevine Phylloxera Management. Department of Natural Resources and Environment Victoria, Australia, pp. 89–98. Powell, K.S., Brown, D., Dunstone, R., Hetherington, S.C. and Corrie, A.M. (2000) Population dynamics of phylloxera in Australian vineyards and implications for management. In: Powell, K.S. and Whiting, J. (eds) Proceedings of the International Symposium on Grapevine Phylloxera Management. Department of Natural Resources and Environment, Melbourne, Australia, pp. 7–20. Powell, K.S., Slattery, W.F., Deretic, J., Herbert, K.S. and Hetherington, S.C. (2003) Influence of soil type and climate on the population dynamics of grapevine

114 phylloxera in Australia. Acta Horticulturae 617, 33–41. Powell, K.S., Bruce, R.J. and Mackie, A.M. (2007a) Optimising Detection and Management Methods for Soil Borne Pest Incursions. Grape and Wine Research Development Corporation Final Report, Australia. Powell, K.S., Burns, A., Norng, S., Granett, J. and McGourty, G. (2007b) Influence of composted green waste on the population dynamics and dispersal of grapevine phylloxera Daktulosphaira vitifoliae. Agriculture, Ecosystems and Environment 119, 33–38. Powell, K.S., Herbert, K.S. and Hoffmann, A.A. (2007c) Grapevine phylloxera – opportunities for monitoring and detection using non-destructive techniques. Australian Viticulture 116, 50–53. Powell, K.S., Trethowan, C.J., Blanchfield, A.L. and Norng, S. (2007d) Composted winery waste and its influence on grape phylloxera in ungrafted vineyards. Acta Horticulturae 733, 143–150. Proffitt, A., Bramley, R., Lamb, D. and Winter, E. (2006) Precision Viticulture – A New Era in Vineyard Management and Wine Production, 1st edn. Winetitles, Adelaide, Australia. Reisenzein, H., Pfeffer, M., Aust, G. and Baumgarten, A. (2007) The influence of soil properties on the development of grape phylloxera populations in Austrian viticulture. Acta Horticulturae 733, 13–23. Renzullo, L.J., Held, A., Powell, K.S. and Blanchfield, A.L. (2004) Remote sensing phylloxera infestation: current capabilities and future possibilities for early detection. Australian and New Zealand Grapegrower and Winemaker 485, 126–130. Renzullo, L.J., Blanchfield, A.L., Guillermin, R., Powell, K.S. and Held, A.A. (2006a) Comparison of PROSPECT and HPLC estimates of leaf chlorophyll contents in a grapevine stress study. International Journal of Remote Sensing 27, 817–823. Renzullo, L.J., Blanchfield, A.L. and Powell, K.S. (2006b) A method of wavelength selection and spectral discrimination of hyperspectral reflectance spectrometry. IEEE Transactions on Geosciences and Remote Sensing 44, 1986–1994.

K.S. Powell Tjallinge, W.F. (1988) Electrical recording of stylet penetration activities. In: Minks, A.K. and Harrewijn, P. (eds) Aphids: Their Biology, Natural Enemies and Control. Elsevier, Amsterdam, The Netherlands, pp. 95–108. Trethowan, C.J. and Powell, K.S. (2007) Rootstock–phylloxera interactions under field conditions. Acta Horticulturae 733, 115–122. Tucker, D.J., Lamb, D.L., Powell, K.S., Blanchfield, A.L. and Brereton, I.M. (2007) Detection of phylloxera infestation in grapevines by NMR methods. Acta Horticulturae 733, 173–181. Turley, M., Granett, J., Omer, A.D. and De Benedictis, J.A. (1996) Grape phylloxera (Homoptera: Phylloxeridae) temperature threshold for establishment of feeding sites and degree-day calculations. Environmental Entomology 25, 842–847. Umina, P.A., Corrie, A.M., Herbert, K.S., White, V.L., Powell, K.S. and Hoffmann, A.A. (2007) The use of DNA markers for pest management: clonal lineages and population biology of grape phylloxera. Acta Horticulturae 733, 183–195. Viduka, K., Mitrovoski, P., Hoffmann, A.A. and Corrie, A.M. (2003) Can phylloxera grow on your rootstocks? Part 2. Australian and New Zealand Grapegrower and Winemaker 476, 55–58. Vorwerk, S. and Forneck, A. (2006) Reproductive mode of grape phylloxera (Daktulosphaira vitifoliae, Homoptera: Phylloxeridae) in Europe: molecular evidence for predominantly asexual populations and a lack of gene flow between them. Genome 49, 678–687. Vorwerk, S., Martinez-Torres, D. and Forneck, A. (2007) Pantoea agglomerans-associated bacteria in grape phylloxera (Daktulosphaira vitifoliae, Fitch). Agricultural and Forest Entomology 9, 57–64. Wildman, W.E., Nagaoka, R.T. and Lider, L.A. (1983) Monitoring spread of grape phylloxera by color infrared aerialphotography and ground investigation. American Journal of Enology and Viticulture 34, 83–94.

7

Using Biocontrol Against Root-feeding Pests, with Particular Reference to Sitona Root Weevils S.L. GOLDSON1 AND P.J. GERARD2 1

AgResearch, Lincoln, New Zealand; 2AgResearch, Hamilton, New Zealand

7.1. Introduction Natural enemies are one of the primary factors that maintain root herbivore equilibria within ecosystems. When a beneficial exotic species is established in a new and/or uncluttered ecosystem in the absence of its co-evolved natural enemies, it often reaches higher populations or has more vigorous growth than in its country of origin. As an island nation, New Zealand has been able to exploit this ecological opportunity resulting in a vibrant economy based on agricultural, forestry and horticultural export industries heavily dependent on exotic plant and animal species. However, the resultant relatively simple productive ecosystems are themselves vulnerable. An example is the New Zealand grass grub, Costelytra zealandica White (Coleoptera: Scarabaeidae). This endemic species has been able to thrive within the exotic ryegrass/clover ecosystem, whereas their natural enemies have not. Indeed, many of these novel ecosystems have been found to be open to subsequent waves of invasive species. As a result, numerous exotic root herbivores have established in New Zealand, some becoming serious pests. In pastoral agriculture, these include the black beetle, Heteronychus arator Fabricius (Coleoptera: Scarabaeidae), from South Africa, white-fringed weevil, Graphognathus leucoloma Boheman (Coleoptera: Curculionidae), from South America and soldier fly, Inopus rubriceps Macquart (Diptera: Stratiomyidae), from Australia. Just as the pest species have thrived through the absence of natural enemies and little competition, the same has been found for recently introduced exotic biocontrol agents. These too, have performed well beyond expectation. The circumstances described above make New Zealand a natural laboratory within which the factors determining the performance of biocontrol agents can be investigated. As a consequence, in-depth studies have been undertaken in association with the successful introductions of two ©CAB International 2008. Root Feeders: An Ecosystem Perspective (eds Johnson and Murray)

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biotypes of the parasitic wasp, Microctonus aethiopoides Loan (Hymenoptera: Braconidae), to control two weevils: first, the lucerne weevil, Sitona discoideus Gyllenhal (Coleoptera: Curculionidae), in the 1980s, and subsequently in 2006 the clover root weevil, S. lepidus Gyllenhal (Coleoptera: Curculionidae). In this chapter, we will use these introductions as case studies to explore the potential of biocontrol agents against root herbivores.

7.2. Potential of Biocontrol as a Management Tool for Root Herbivores The introduction of M. aethiopoides into New Zealand is an example of classical biocontrol, which is defined as ‘the intentional introduction of an exotic biocontrol agent for permanent establishment and long-term pest control’ (Eilenberg et al., 2001). By importing and releasing one or more of the coevolved natural enemies of a pest, the aim is to establish a self-regulating control that will maintain pests at equilibria below economic or environmental significance. Given the inherent difficulty in undertaking research on root herbivores, let alone their natural enemies, by far the majority of classical biocontrol programmes have been aimed at aboveground pests. For instance, as in 2001, of the 98 arthropod pests or groups of pests which had been the subject of biocontrol projects in Australia, only two were root herbivores (cane grubs and S. discoideus) and two more attacked tubers (Waterhouse and Sands, 2001). Biocontrol of root herbivores shares the same useful characteristics of aboveground pests in that there are none of the risks associated with synthetic pesticide toxicity, residue or resistance problems. In the case of classical biocontrol, the introduced natural enemy usually extends itself over large areas, including inaccessible sites; indeed, once established it is selfperpetuating and freely available to all. As long as thorough research for possible direct and indirect harmful effects on non-target organisms is undertaken beforehand, biocontrol agents target the host pest species and do not harm the environment. Biocontrol of root herbivores has some additional advantages beyond those found in aboveground pests. In most production systems, the roots are not the marketable component. Therefore, the low herbivore populations that are maintained in a successful biocontrol programme are tolerable, and may even be beneficial in enhancing nutrient cycling and/or encouraging the growth of new, more efficient roots. Also, the soil provides protection from ultraviolet radiation and desiccation, enabling insect pathogenic microbes and nematodes to be exploited for biocontrol purposes. Shortcomings often attributed to biocontrol may not be as acute for root herbivores as for aboveground pests. Although natural enemies may be slow-acting and therefore not necessarily as immediately effective as chemical controls, the latter often are unsatisfactory for root herbivores. Many insecticides are deactivated after contact with soil, and those that are not (due to persistence) can lead to residue problems in both food and the environment. There is also the considerable attendant difficulty in monitoring

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pest population treatment thresholds, and prophylactic treatments tend to be costly and engender pest resurgence and pesticide resistance. Biocontrol is a particularly attractive option to control forage pests in New Zealand. The forage plants can tolerate low herbivore populations and cosmetic damage is of no consequence. There is also little use of pesticides against forage pests because of the cost of treating large areas combined with stringent international controls on residues in farm produce. As a result, there is minimal likelihood of biocontrol disruption through pesticide impacts. Finally, forage crops and pastures are usually perennial systems that permit stable host–prey relationships, although there can be some disturbance through grazing or mowing. Root herbivores pose their own challenges in terms of achieving effective biocontrol. First, there is a paucity of knowledge on belowground intraspecific and interspecific interactions. While there is increasing recognition of the role that root herbivores have in productive and natural ecosystems, the inherent difficulties in undertaking research on subterranean interactions deter all but the most resolute investigators. Second, it is usually difficult to locate root herbivores, let alone their natural enemies, in such a habitat. The presence and impact of known root herbivore pest species often goes undetected in production and natural ecosystems, and even the sudden appearance of dead plants may be wrongly attributed to interacting factors such as drought. Third, root herbivores, especially those found within the roots, occupy a relatively safe refuge from those parasitoid families associated with aboveground herbivores. While 75% of known parasitoid species are Hymenoptera, the evolution of parasitism within the Order is closely tied to vegetation-zone habitats, which offer little opportunity for activity against soil-dwelling hosts (Eggleton and Belshaw, 1993). Conversely, most dipteran parasitoids arose from saprophagous ancestors, with ancestors and hosts that live in or near the soil surface. While many dipteran parasitoids may attack root herbivores, research into their application as control agents is challenging. Parasitism has evolved independently, perhaps >100 times, in 21 dipteran families, and as a consequence, host–parasitoid interactions involving this group are themselves diverse and multifaceted (Eggleton and Belshaw, 1993). Host location of root feeders is generally partitioned into two phases with adult females locating the general vicinity of a potential host, scattering eggs or larvae on the soil surface and then departing, leaving the young larvae to actively seek the host. With the complexity of the biology and ecology and the high level of polyphagy among Tachinidae (Feener and Brown, 1997), dipteran parasitoids are usually not attractive candidates for classical biocontrol programmes. In their review of scarabs as pests, Jackson and Klein (2006) noted that, although insect parasitoids can be found attacking larvae, they are not usually abundant in scarab populations. This is probably true for most root herbivore species. The most common parasitoid families are Tachinidae (Diptera) and Tiphiidae and Scoliidae (Hymenoptera). It is quite possible that the relative lack of success of these parasitoid families in biocontrol programmes is that as well as having specialized behaviours to find their subterranean hosts,

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the adults appear to be dependent on honeydew and nectar sources. For example, parasitism of the Japanese beetle, Popillia japonica Newman (Coleoptera: Scarabaeidae) by the tiphiid wasp Tiphia vernalis Rohwer (Hymenoptera: Tiphiidae) has been found to be greatest when adjacent to either a good nectar source or honeydew of aphids associated with oaks and maples (Rogers and Potter, 2004). In contrast to the modest opportunity offered by parasitoids, there are many different pathogens and nematodes associated with soil-dwelling larvae. Root herbivores can be attractive targets for biocontrol using microbes as the generalized pattern shown by many pest species is steady population growth, resulting in high densities. In addition to long-term occupation of sites that foster the horizontal transmission of pathogens within generations, vertical transmission can occur between generations (Jackson and Klein, 2006). In spite of the potential, relatively few insect pathogens have the appropriate attributes to be successful control agents of root herbivores (Jackson et al., 2000). Two key factors have been found to be important in microbial control: specificity and environmental competence (Jackson, 1999). Root herbivores are remarkably resistant to generalist entomopathogens and the most successful agents are usually highly specific pathotypes that have coevolved with the target host (Jackson, 1999). Further, soil is an extremely competitive environment and a microbial agent must be able to establish, persist and infect target hosts in sufficient numbers to ensure an epizootic develops. Finally, the agent must be amenable to production and distribution.

7.3. Case Study One – Successful Biocontrol Targeting Belowground Stages: Control of the Citrus Root Weevil by Entomopathogenic Nematodes in Florida The citrus root weevil Diaprepes abbreviatus L. (Coleoptera: Curculionidae) is the most serious pest of citrus in Florida, costing the industry around US$75 million each year. It originated from the Caribbean and, since its discovery in 1964, has spread throughout the Florida peninsular and north to approximate latitude 29°N (Lapointe et al., 2007). The combination of larval root herbivory and subsequent fungal infection through wounds on the major roots debilitates and even kills trees. Damage is greatest in poorly drained soils that provide ideal conditions for fungi such as Phytophthora spp., while orchards on deep, well-drained, sandy soils suffer less damage. The weevil is polyphagous, with adults feeding on the foliage of over 250 species. The eggs are laid in clusters between foliage glued together and D. abbreviatus females typically lay around 2000 eggs each (Nigg et al., 2004). The neonate larvae drop to the ground to feed on roots for several months before pupating in the soil. With adults emerging from late spring into autumn and the prolonged oviposition period, control with non-persistent pesticides is difficult and cultural and biocontrol strategies play an important role in the management of pest populations.

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Classical biocontrol efforts using egg parasitoids have been largely unsuccessful thus far with little evidence of widespread establishment of the three species of egg parasitic wasps, Quadrastichus haitiensis Gahan (Hymenoptera: Eulophidae) (1969–1971), Ceratogramma etiennei Delvare (Hymenoptera: Trichogrammatidae) (1998) and Aprostocetus vaquitarum Wolcott (Hymenoptera: Eulophidae) (1999) introduced from the Caribbean (Frank and McCoy, 2007). While Q. haitiensis and A. vaquitarum have established in extreme south-eastern Florida, they are absent from the main commercial citrus-growing areas in central Florida. These species require a continuous supply of fresh D. abbreviatus egg masses, which appears to limit them to areas where mean daily air temperatures do not fall below 15°C more than 25 days a year (Lapointe et al., 2007). In contrast, inundation biocontrol using entomopathogenic nematodes (EPN) appears to be a useful tool in the central ridge area of Florida. Commercial formulations of the exotic nematode Steinernema riobrave and an endemic strain of Heterorhabditis indica have been available since the mid1990s. Inundation biocontrol is ‘the use of living organisms to control pests when control is achieved exclusively by the release organisms themselves’ (Eilenberg et al., 2001). D. abbreviatus is a good candidate for this form of control in that citrus is a relatively high value crop, the larvae are present year round, and nematode applications are targeted at the root zone under the canopy where they are protected from ultraviolet radiation. However, levels of D. abbreviatus control using EPN treatments are variable and studies have been undertaken on aspects of the soil ecosystem to provide better understanding. EPN applications have greatest efficacy in the deep, coarse-textured sandy soils found on the north–south central ridge of the Florida peninsula, and have erratic efficacy on soils with a fine texture, especially if compacted (McCoy et al., 2002). The abundance and diversity of endemic EPN have been found to be similarly favoured by coarse sandy soils, and to be implicated in the regional patterns of D. abbreviatus abundance and damage in Florida (Duncan et al., 2003). Applying treatments of the relatively short-lived S. riobrave to central ridge soils consistently increases D. abbreviatus mortality, but also increases the prevalence of nematophagous fungi, which in turn can temporarily suppress the long-lived endemic EPN (Duncan et al., 2007). These non-target effects could limit the cost–benefits of using EPN applications in regions where control by endemic EPN is ordinarily high. However, if applications were timed immediately following peaks of larval recruitment, the potential of disruption would be minimized (Duncan et al., 2007).

7.4. Biocontrol of Root Herbivores Targeted at Aboveground Life Stages In many cases targeting the belowground stages is not effective. They may be present for only a few months a year and it may be impossible to find effective natural enemies that can bridge the intervening period (e.g. acceptable

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alternate host, diapause to obtain synchrony with host life cycle and resilient spores). The root feeders may not be accessible because of the depth at which they feed or because they are protected within galls or other root structures. However, parasitoids targeting either eggs or adults can be a useful option. A caveat to this though is that successful establishment and even moderate levels of host mortality may have no impact on pest populations. Many root-feeding pests are very fecund and have very high levels of egg and neonate larval mortality arising through desiccation, predation and competition for feeding sites. In these circumstances, it is unlikely that an egg parasitoid would be able to reach sufficiently high levels to impact on the abundance of larvae establishing belowground, especially if eggs are laid singly, and not in batches. However, a natural enemy that can prevent oviposition by rendering the adult pest immobile or sterile can reduce root herbivore abundance if it has a high searching efficacy and is fecund.

7.5. Case Study Two – Successful Biocontrol Targeting Aboveground Life Stages: Control of Sitona Weevils Using M. aethiopoides in New Zealand 7.5.1. Pest status and phenology of Sitona spp. in New Zealand Sitona Germar is a large genus, with more than 100 species originating in the Nearctic and Palaearctic regions (De Castro et al., 2007). All feed on Fabaceae (Leguminosae) in particular medicks (Medicago spp.) and clovers (Trifolium spp). New Zealand has been invaded by two Sitona spp.: first, S. discoideus in the 1970s, which attacks lucerne crops and medicks, and more recently, S. lepidus in the 1990s, which attacks white clover. On arrival, both species, but particularly S. lepidus, were presented with almost ideal conditions for an r-strategist (MacArthur and Wilson, 1967) with high fecundity, strong flight capability, few natural enemies and with relatively lengthy longevity. The New Zealand agricultural ecosystem offers a spatial continuum of highly favourable habitats constituting of perennial pastures containing clovers and medicks. Notably, there were no other competing insect populations using the root nodules as a resource. Within two years of its discovery in the North Island in 1974 (Esson, 1975), S. discoideus had spread throughout New Zealand reaching pest proportions in lucerne Medicago sativa L. in the South Island (Somerfield and Burnett, 1976). S. lepidus has been found to have a slower rate of dispersal having taken c.10 years to reach the South Island. Sitona spp. adults feed on the foliage, while the larvae feed on the root nodules and roots. A study of the impact of S. discoideus on lucerne production in the South Island showed that while adult defoliation was far more obvious, it only accounted for 25% of mid-season production compared to a loss of 43% that was attributable to root herbivory (Goldson et al., 2005). Considering seasonal production, a sharply defined damage threshold occurred at the point where photosynthetic capability collapsed. This is conjectured to be related to the stage when the nitrogen used to replace nodules

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lost under severe larval attack exceeded that being fixed by surviving nodules (Goldson et al., 1987). Soil type, rather than climate, appeared to be the main factor accounting for regional differences in pest status, with greatest damage in shallow, free-draining soils subject to leaching of mineralized nitrogen (Worner et al., 1989). Later studies on S. lepidus root herbivory showed a similar damage threshold and the ability to shift plant physiology from vegetative to reproductive growth (Gerard et al., 1999). Typical postinvasive S. lepidus populations in ryegrass/white clover pastures, and in the presence of other root herbivores, were shown to depress clover production by around 35% during spring (Gerard et al., 2007). The two Sitona spp. differ in life cycle. S. discoideus shows univoltine aestivatory behaviour reflecting its Mediterranean origin. The adult emergence commences in early summer, whereupon they migrate to aestivation sites for the hottest part of the summer. Migration back to feeding sites occurs in the autumn and oviposition commences subsequently (Goldson et al., 1984). The eggs are laid throughout the winter into spring. Larval numbers peak in spring and this coincides with the period of maximum nitrogen demand by the crop. S. lepidus is Palaearctic in origin and the number of generations a year is dependent on temperature. Unlike in Europe where it is generally univoltine, in northern New Zealand there are two overlapping generations a year. Adults commence emergence in mid to late spring and produce a summer generation of larvae (see Fig. 7.1). These emerge as adults in autumn and give rise to a winter generation of larvae. As the adults are relatively longlived and remain active both in summer and winter, adults and larvae can be found throughout the year (Gerard et al., 2007). Prior to the release of M. aethiopoides, instances of parasitism and disease were very uncommon in field populations of S. discoideus in both Australia (Waterhouse and Sands, 2001) and New Zealand (Wightman, 1986) and had no impact whatsoever. As with S. humeralis Stephens (Coleoptera: Curculionidae) in Mediterranean climatic areas (Aeschlimann, 1979), the greatest mortality in S. discoideus and S. lepidus occurred immediately after hatching in part as the result of generalist predation, desiccation and competition for root nodules.

7.5.2. Parasitoid selection S. discoideus came to New Zealand via Australia where it had become a major pest of annual medick pastures and lucerne by the early 1970s. Aeschlimann (1979) undertook a study of Sitona spp. and their natural enemies in southern Europe and northern Africa and identified M. aethiopoides and the tachinid, Microsoma exigua Meigen (Diptera: Tachinidae) as significant mortality factors in adult populations. Using life table data from Australia and Europe, Aeschlimann (1979) concluded that natural enemies attacking the preimaginal stages or suppressing the weevil’s fecundity should be given first priority for release in Australia. M. aethiopoides is an endoparasitoid of adult weevils from the genera Sitona and Hypera. This control agent has the desirable attribute of rendering female

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(A)

Overwintering (eggs/larvae/adults)

Sitona lepidus (Europe)

D

J F

N

Walking dispersal to new sites

O

M

S

A M

A

Oviposition

J New single generation of adults (B)

Overwintering adults become active

J

Oviposition by overwintering adults

Flight dispersal to new sites

New generation of adults

D

Sitona lepidus (New Zealand)

J

Multiple generations (≥3)

F

N O

M

S

A A

M J

J

Overwintering (eggs/larvae/adults)

Fig. 7.1. Comparative life cycles of Sitona lepidus in (A) Europe and (B) New Zealand.

weevils sterile shortly after the parasitoid egg is deposited in the weevil’s haemocoel (Loan and Holdaway, 1961). M. aethiopoides can complete its life cycle in 2 Mg ha−1 year−1 in a deciduous hardwood stand in the Adirondack Mountains (Burke and Raynal, 1994), and exceeded 4 Mg ha−1 year−1 in sugar maple, Acer saccharum, stands in Wisconsin (Aber et al., 1985). Average belowground NPP is 7 Mg ha−1 year−1 in temperate forest systems (Burrows et al., 2003). Belowground herbivory can have numerous effects at scales of individual plant roots and shoots, plant communities and ecosystems (see Blackshaw and Kerry, Seastedt and Murray, Hunter and Johnson et al., Chapters 3, 4, 5 and 9, respectively, this volume). Root feeders often decrease the belowground biomass and alter the physiology of their host plant, and may exert a significant influence on primary production (Detling et al., 1980). Stevens et al. (2002) proposed root herbivory as the leading explanation for 37% fineroot mortality in a longleaf pine, Pinus palustris Miller, stand. Consistent with this hypothesis, an insecticidal soil drench increased fine-root longevity by up to 125 days, and decreased fine-root mortality by as much as 41% in peach, Prunus persica Batsch, trees (Wells et al., 2002). 134

©CAB International 2008. Root Feeders: An Ecosystem Perspective (eds Johnson and Murray)

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Root density and surface area are correlated with a plant’s competitive ability to gather water and nutrients (Casper and Jackson, 1997). Belowground herbivory can reduce competitive abilities, which can be particularly important at high plant densities. The relationship between root herbivory and competitive ability was demonstrated in purple loosestrife, Lythrum salicaria L. (Nötzold et al., 1998), where Hylobius transversovittatus Goeze (Coleoptea: Curculionidae) delayed flowering and reduced plant height, shoot weight and total biomass. In addition, fine-root feeders can greatly alter the carbon and nutrient flow throughout a habitat (Blossey and Hunt-Joshi, 2003), as fine roots generally have the highest nitrogen concentration, an essential element for insect development (Scriber and Slansky, 1981). Despite the importance of belowground herbivory, little is known about native species in natural systems. The majority of our knowledge of belowground herbivores is from studies of pests of turf, agriculture and plantation forests. Of these, the corn rootworm, Diabrotica spp. (Coleoptera: Chrysomelidae), complex is probably the most damaging root feeder in agricultural systems worldwide, costing North American farmers over US$1 billion annually (ARS, 2001). Another well-studied example involves red pine, P. resinosa Solander, decline and Christmas tree mortality in the mid-western USA (Rieske and Raffa, 1993; Erbilgin and Raffa, 2002). There are few well-studied rhizophagous pests in natural systems in North America, with cicadas (Hemiptera: Cicadidae) being one exception (see Hunter, Chapter 5, this volume).

8.1.2. Invasive species Biological invasions constitute one of the greatest threats to native biodiversity (Gurevitch and Padilla, 2004), being partially responsible for nearly 50% of extinct or imperiled species in the USA (Wilcove et al., 1998). They cost the US economy an estimated US$120 billion annually (Pimentel et al., 2005), and may persist undetected for years before discovery (Liebhold et al., 1995; Mattson et al., 2007). Invasive plants such as kudzu, Pueraria spp., cost the USA nearly US$500 million annually, and salt cedar, Tamarix spp., can outcompete native flora, reduce the available groundwater (Hoddenbach, 1987) and reduce resident nesting bird species by >97% (Anderson and Ohmart, 1977). Invasive pathogens cost the USA an estimated US$30 billion year−1. For example, the exotic fungi causing Dutch elm disease (Ophiostoma spp.), white pine blister rust (Cronartium ribicola J. C. Fisch. ex Rab) (Peterson and Jewell, 1968; Gibbs and Wainhouse, 1986), butternut canker (Sirococcus clavigigenti-juglandacaerum N. B. Nair, Kostichka and Kuntz) (SAMAB, 1996), chestnut blight fungus (Cryphonectria parasitica [Murrill] M. E. Barr) (Liebhold et al., 1995) and sudden oak death (Phytophthora ramorum S. Werres, A. W. A. M. De Cock) (Rizzo et al., 2002) have dramatically and irrevocably altered ecosystem structure, composition and function. Arthropods are one of the major groups of invasive species in North America, and have had enormous economic and ecological effects. Forests

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are particularly susceptible to exotic insect invasions, partially because of the vast area and diverse ecosystems they cover. There are many well-documented cases of invasive insects in US forests (Mattson et al., 1994), but, nearly all published examples are aboveground feeders. Folivores such as the gypsy moth, Lymantria dispar L. (Lepidoptera: Lymantriidae), can alter species composition of mature forests under heavy, repeated defoliation, and reduce aesthetic values of parks and urban areas (Liebhold et al., 1995). The hemlock wooly adelgid, Adelges tsugae Annand (Homoptera: Adelgidae), threatens to eliminate hemlocks from eastern US forests (Orwig and Foster, 1998). Recently, the woodwasp, Sirex noctilio Fabricius (Hymenoptera: Siricidae), was discovered in New York (Hoebeke et al., 2005), subjecting several Pinus spp. to potential infestation and mortality. Aboveground insects have received the vast majority of attention worldwide because they are more apparent, and their aboveground life histories make them easier to study. The number of known invasive aboveground insects dwarfs the number of invasive belowground insects. For example, www.invasive.org lists 223 invasive insect species – of which only six are belowground pests. Less than 10% of the 423 exotic phytophagous insects in North American forests are root feeders (Mattson et al., 1994, 2007). In Canada, Kimoto and Duthie-Holt (2006) list 41 exotic forest insect species, of which only four feed belowground. Just as belowground herbivory by native insects is largely underestimated (Blossey and Hunt-Joshi, 2003), the same is likely true for invasive species. Again, our knowledge is derived mainly from cultivated systems. In North America, the major invasive root-feeding agricultural pest is the clover root curculio, Sitona hispidulus Fabricius (Coleoptera: Curculionidae), causing yield losses of nearly 1 Mg ha−1 (Hower et al., 1995). The Japanese beetle, Popillia japonica Newman (Coleoptera: Scarabaeidae), feeds on more than 300 plant species in the USA and costs over US$450 million each year for control and management (Mannion et al., 2001; Potter and Held, 2002). The black vine weevil, Otiorhynchus sulcatus Fabricius (Coleoptera: Curculionidae), is a serious pest of many ornamental tree species and small fruits (Moorhouse et al., 1992). The sugarcane rootstalk borer, Diaprepes abbreviatus L. (Coleoptera: Curculionidae), has recently been found on the West Coast of North America (Grafton-Cardwell, 2005), and threatens to severely impact plant production. The sweet potato weevil, Cylas formicarius Fabricius (Coleoptera: Brentidae) (Chalfant et al., 1990), European crane fly, Tipula spp. (Diptera: Tipulidae) (Umble and Rao, 2004) and several scarabs (Coleoptera: Scarabaeidae) (Jackson and Klein, 2006) are also economically important invasive belowground pests in North America. Although an insect’s economic impact often drives the research, its environmental impact can be equally important. For example, a suite of invasive root-feeding weevils (Coleoptera: Curculionidae) has established in the northern hardwood forests of eastern North America, and research has just begun to determine their range and impact. In this chapter, we summarize what is known so far about these insects, discuss their impacts on the northern forest ecosystems and suggest future research strategies and directions.

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8.2. Invasive Root-feeding Weevils in Eastern North American Deciduous Forests 8.2.1. Species composition A complex of nine invasive rhizophagous weevils has been found by various trapping methods in northern hardwood forests in the north-eastern and Great Lakes Regions of North America. Two of these, Polydrusus sericeus Schaller and Phyllobius oblongus L., are generally the most abundant, comprising >80% of the total weevil population (Pinski et al., 2005b; D.R. Coyle, 2008, unpublished data). The other species, in order of relative abundance, include Sciaphilis asperatus Bonsdorff, Barypeithes pellucidus Boheman, Trachyphloeus aristatus Gyllenhal and O. ovatus L. (Pinski et al., 2005b; D.R. Coyle, 2008, MI, unpublished data). Pitfall trapping recently yielded two additional invasive species, Calomycterus setarius Roelofs and Pachyrhinus elegans Schoenherr (Werner and Raffa, 2000), and sticky traps yielded the most recently discovered species, Strophosoma melanogrammum Forster (Shields et al., 2008). Only two native species have been found so far: H. warreni Wood via pitfall trapping (Werner and Raffa, 2000) and Hormorus undulates Uhier via sweepnetting. While there is some variation in phenology, the life cycles of these species are very similar. Adults emerge in late spring and early summer. They have an obligatory pre-oviposition feeding period on the developing buds and leaves of various understory deciduous woody plants, especially seedlings and saplings of sugar maple, hop hornbeam, Ostrya virginiana Koch, yellow birch, Betula alleghaniensis Britton, basswood, Tilia americana L. and various shrubs including raspberry (Rubus spp.). Their impact on the leaf surface area of these plants can be severe, at times approaching 100% defoliation. Mating takes place soon after emergence and oviposition occurs approximately 2 weeks later, when eggs are deposited near or into the soil. Larvae hatch in approximately 1 month and begin feeding on root tissue. Larvae overwinter in the soil, and resume feeding the following spring until they pupate in May. Larval feeding habits and host preferences are, for the most part, unknown. However, we do know that some larvae do not enter a winter diapause, particularly if snowpack prevents a deep soil freeze. Preliminary data show that even over winter, some new fine roots are produced by trees and larvae recovered during the winter months were active and increasing in weight, suggesting growth even during the winter months. Yet overall, little is known about the larval ecology and their feeding impacts on the invaded ecosystems. 8.2.2. Adult host range Like many invasive coleopterans that feed on woody plants, including scarabs (Reding and Klein, 2007) and Otiorhynchus root weevils (Van Tol et al., 2004; Fisher, 2006), this suite of nine European weevils is polyphagous, feeding on many species of trees and shrubs. Phyllobius oblongus is known to feed

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on elm (Ulmus spp.), maple (Acer spp.), birch (Betula spp.), hop hornbeam, aspen (Populus tremuloides), willow (Salix spp.), basswood, pear (Pyrus spp.), apple (Malus spp.), various shrubs and strawberries (Fragaria spp.) (Felt, 1928; Massee, 1932; Caruth, 1936; Fields, 1974; Helsen and Blommers, 1988). Hop hornbeam and mountain maple (A. spicatum Lamarck) were preferred in laboratory trials, followed by basswood, white birch (Betula papyrifera Marshall), sugar maple, red maple (A. rubrum), aspen, poplar (Populus) and yellow birch (Pinski et al., 2005a). P. sericeus feeds not only on many of the same aforementioned hosts, but also on oak (Quercus spp.), hazel (Corylus spp.) and alder (Alnus spp.) (Parrott and Glasgow, 1916; Frost, 1946; Simmons and Knight, 1973; Morris, 1978; Casteels and De Clercq, 1988; Gharadjedaghi, 1997). In laboratory feeding trials, yellow birch and basswood were the most preferred host species, followed by hop hornbeam, white birch, red oak (Quercus rubra), poplar, aspen, sugar maple, mountain maple and red maple (Pinski et al., 2005a). The generalist B. pellucidus feeds on strawberry (Bomford and Vernon, 2005), raspberry (Levesque and Levesque, 1994) and grapes (Vitis spp.) (Bouchard et al., 2005). This is a widely distributed invasive weevil, and is known to feed on hosts from the plant families Anacardiaceae, Asteraceae, Fagaceae, Rosaceae, Ulmaceae, Vitaceae (Bouchard et al., 2005) and Cucurbitaceae (Barrett and Agrawal, 2004). Interestingly, B. pellucidus is an important component of salamander diets in the north-eastern USA (Maerz et al., 2005). Sciaphilis asperatus feeds primarily on sugar maple, birch, raspberry and other trees and shrubs (Henshaw, 1888; Witter and Fields, 1977; Levesque and Levesque, 1994; Maerz et al., 2005), as well as plants in the family Apiaceae (Šerá et al., 2005). In addition, we have captured S. asperatus on hop hornbeam and basswood. Hosts commonly consumed by both P. oblongus and P. sericeus (and presumably by S. asperatus) in the northern hardwood forest include sugar maple, red maple, hop hornbeam, elm, basswood and wild raspberry. Leatherwood, Dirca palustris L., is almost never eaten even though it is relatively common. Few records of T. aristatus exist, but these weevils are occasionally found in northern hardwood forests (Pinski et al., 2005a). Trachyphloeus bifoveolatus, a close relative, is reported to be a common pest of grasslands (Barstow and Getzin, 1985), raspberries (Levesque and Levesque, 1994) and vineyards (Bouchard et al., 2005).

8.2.3. Geographic distribution Without aggressive and systematic sampling, determining an accurate geographic range for any insect species is extremely difficult. None the less, with the help of many insect museum curators across the north-eastern and midwestern USA, and eastern Canada, we have compiled what we believe is an accurate picture of the current distribution of this suite of invasive weevils (Table 8.1). Due to the low numbers of T. aristatus and O. ovatus captured, we

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Table 8.1. Confirmed collection locations of invasive root-feeding weevils in North America. See text for references. Species

USA

Canada

Phyllobius oblongus

Connecticut, Michigan, Minnesota, New Hampshire, New York, Ohio, Pennsylvania, Wisconsin, West Virginia Connecticut, Illinois, Indiana, Massachusetts, Michigan, Minnesota, New Hampshire, Ohio, Pennsylvania, Wisconsin California, Connecticut, District of Columbia, Idaho, Illinois, Indiana, Massachusetts, Maryland, Maine, Michigan, Minnesota, North Carolina, New Hampshire, New Jersey, New York, Ohio, Oklahoma, Oregon, Pennsylvania, Rhode Island, Utah, Virginia, Vermont, Washington, Wisconsin, West Virginia Colorado, Connecticut, Idaho, Massachusetts, Maryland, Maine, Michigan, Minnesota, North Carolina, New Hampshire, New Jersey, New York, Ohio, Oklahoma, South Dakota, Vermont, Wisconsin

New Brunswick, Nova Scotia, Prince Edward Island, Quebec

Polydrusus sericeus

Barypeithes pellucidus

Sciaphilis asperatus

New Brunswick, Nova Scotia, Ontario, Prince Edward Island, Quebec British Columbia, New Brunswick, Newfoundland, Nova Scotia, Ontario, Prince Edward Island, Quebec

Alberta, British Columbia, New Brunswick, Nova Scotia, Ontario, Quebec

will focus on P. sericeus, P. oblongus, B. pellucidus and S. asperatus. Several references were also used in constructing these ranges (Arnett, 1973; O’Brien and Wibmer, 1982; Wibmer and O’Brien, 1989; Majka et al., 2007a,b) as well as the generous help from nearly 20 public and University museum curators. P. oblongus was first recorded in New York, USA, in 1923 (Felt, 1928). It has been captured in eastern Canada, throughout the north-eastern USA, south to West Virginia and west to Minnesota, where it was first collected in 1990. P. sericeus, first discovered in Connecticut in 1934 (Britton, 1934), has been captured in every state and province bordering the Great Lakes, several north-eastern US states and in the Maritime Provinces of Canada. S. asperatus was first captured in Nova Scotia in 1884 (Harrington, 1891). Currently, it is well established in the north-eastern USA, and there are scattered records of its occurrence across much of southern Canada and the northern USA, including as far south as Oklahoma and North Carolina. B. pellucidus has the most cosmopolitan distribution of this group, having

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been collected in all the Maritime Provinces of Canada and Quebec, Ontario and British Columbia. Blatchley and Leng (1916) first reported this weevil in several north-eastern states in the early 1900s. Barypeithes pellucidus has been recorded from nearly all states in the north-east and bordering the Great Lakes, and as far south as North Carolina and Oklahoma, and in several states west of the Rocky Mountains.

8.2.4. Population dynamics We annually monitored larval abundance of the soil-inhabiting invasive weevil complex in the Ottawa National Forest in Gogebic County of the western Upper Peninsula of Michigan from 1998 to 2007. Each November we extracted 30–40 randomly placed soil cores (6.45 cm diameter × 16 cm length) from the same 100 × 40 m quadrat of a northern hardwood forest dominated by a dense canopy of mature sugar maple (Pinski et al., 2005a). Soil cores were stored in plastic bags and returned to the laboratory, where we sieved them to recover all meso-macro invertebrates, but especially weevil larvae. All larvae were counted and then saved to measure fresh and dry weights and retained in 80% ethanol for later sorting to species. Weevil larval populations varied yearly by nearly tenfold, and ranged from 112 to 972 m−2 (Fig. 8.1A). Their annual mean density was 571 m−2. Larval fresh mass per square metre varied yearly and ranged almost 14-fold, from 0.52 to 7.11 g m−2, with a 10-year mean of 3.62 g m−2 (Fig. 8.1B). If weevil larvae are randomly distributed within the forest, then the data from our soil cores should conform to the Poisson probability distribution where the sample variance (v2) is equal to the sample mean (v2 = m) (Sokal and Rohlf, 1995). However, Fig. 8.2 reveals instead that sample variances were generally larger than the mean, and increased approximately as follows: v2 = m + m2/k, where k = 3, the variance equation for the negative binomial probability distribution. The parameter k is an index of over-dispersion or aggregation due perhaps to the heterogeneous distribution of larval foods and to behaviour such as egg dumping by mothers. But, should the k values be very large or very small, then the underlying data would likely represent the Poisson or the logarithmic distributions, respectively.

8.3. Impacts on Forest Ecosystems 8.3.1. Soil processes In order to determine the effects that root feeding is having on northern hardwood forests we need to know how much root tissue the larvae are consuming. We can estimate this quantity using larval weights from our 10-year larval sampling data (Fig. 8.1A and B). The larvae were probably only twothirds grown in November, having yet to finish their feeding and final growth in the ensuing spring after soil temperatures permitted feeding. Assuming

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Numbers per m2

1000 800 600 400 200 (B)

Grams fwt per m2

10 9 8 7 6 5 4 3 2 1 0

1998

1999

2000

2001

2002

2003

2004

2005

2006

2007

Year

Fig. 8.1. Annual estimates of (A) larval weevil density and (B) total weevil larval biomass at Taylor Lake, Gogebic Co., Michigan. The dashed line in (B) is the overall mean. Sampling was conducted in November of each year.

Variance

20

10 V 2 = m + m 2/k where k = 3

0

0

1

2

3

4

5

6

Mean larval density/soil core

Fig. 8.2. Relationship between sample variance and mean of larval root-feeding weevil abundance. Sampling was conducted at Taylor Lake, Gogebic Co., Michigan, each November during 1998–2007.

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that the gross efficiency of food conversion for larvae feeding on fine roots is about 5–10% (Slansky and Scriber, 1985), then average total plant consumption by November is roughly 10–20 times fresh larval mass, or 36–72 g m−2 fresh root weight. Furthermore, assuming that fine-root net primary production averages about 200 g m−2 dry weight in northern hardwood forests (Burke and Raynal, 1994), then weevils may be consuming up to 15% of fineroot mass after accounting for their spring feeding. Little information is available on how root herbivory affects soil microbial communities. One approach for measuring soil microbes is phospholipid fatty acid analysis, where lipids of the microbe cell walls are removed and measured, giving an indication of the relative abundance and types of microbes present in the sample (Kao-Kniffin and Balser, 2007). As root herbivory increases, the amount of dead root tissue may increase, as roots may be severed or only partially eaten. An increased number of herbivores will result in an increased amount of frass in the soil, and Hunter (2001a) showed that elevated frass inputs to the soil can drastically alter soil microbiota. The soil microbial community is expected to respond positively to changes in amount and quantity of available organic matter. Herbivory reduces the amount of plant material in the soil, therefore reducing the amount of plant material that will eventually die (e.g. fine-root turnover). This can induce a chain reaction of lower carbon accumulation and reduced carbon flow in an ecosystem (Cebrián and Duarte, 1995), unless grazing stimulates compensatory plant growth. Most carbon balance and nitrogen cycling models do not take root herbivory into account even though it may greatly alter the flux of carbon from naturally dying plant material into the ecosystem. In addition, few soil respiration studies include and identify inputs from soil dwelling fauna, even though this guild is an important contributor to overall soil respiration (Hanson et al., 2000). Fine-root turnover represents a large source of soil carbon accumulation, and is often nearly as high as fineroot production (McClaugherty et al., 1982). Root herbivory by weevil larvae could drastically alter this balance by accelerating root turnover, decreasing aboveground productivity and altering soil carbon fractionization pools. Högberg et al. (2001) showed that a high proportion of plant carbon allocation is belowground, suggesting that nutrient cycling and energy fluxes through terrestrial ecosystems are larger than previously thought. Estimates of global root turnover and primary production may also be greatly underestimated (Chapin and Ruess, 2001), in part due to the paucity of data on the impact of root herbivores. More detailed, intensive and systematic measurement of the impact of root herbivores could lead to a fundamental paradigm shift in our understanding of their roles in root turnover and nutrient cycling.

8.3.2. Displacement of native fauna In the Lake States, invasive curculionid larvae comprise between 75% and 82% of the belowground insect mesofauna (Pinski et al., 2005a,

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D.R. Coyle, 2008, unpublished data). Less than 1% of the larval curculionids were from native species. Invasive weevil adults likewise dominate aboveground arthropod fauna in the understory. Considering the overwhelming proportion of larval curculionids to total fauna, and the ratio of invasive to native root weevils, we can confidently say this suite of invasive weevils is the dominant belowground and aboveground fauna in this system. This raises the question: before the weevils’ introduction to North America, what organisms dominated the belowground ecological niche? While it is possible that prior to the introduction of these invasive weevils there was no root-feeding guild in this ecosystem, this seems unlikely. A more probable scenario is that a native complex of root feeders was replaced by a complex of invasive species that were more efficient competitors. Some evidence supports this idea, namely the rare capture of native weevil species. Curculionid collections in insect museums throughout the range of the northern hardwood forests may hold the answer to this question. If displacement of native species occurred, we would expect the ratio of native to exotic weevils to decline precipitously with collection date. This shows the need for biological surveys that yield baseline data and studies that utilize the resources available in insect museums across North America and worldwide.

8.3.3. How are community processes and forest structure affected? In northern hardwood forests, root feeding by weevils may reduce seedling vigour and increase mortality, reducing regeneration and eventually changing forest structure. Larval weevil feeding on fine roots may indirectly select for more grazing-tolerant plant species or genotypes, as plant tolerance likely varies among individuals. It is unknown if larval weevils feed selectively on the roots of seedlings or mature trees, or show no preference. Given few reports of physiological differences between the fine roots of mature versus young trees, it seems unlikely that larvae have major preferences between them. Wounds caused by root feeding may result in elevated susceptibility or access to pathogens. The soil is rich in microorganisms, and part of a tree’s defences is the protective epidermis on fine roots. Root feeding damages this tissue, creating infection courts. Root feeding by larvae may weaken plants, and reduce their competitive ability to compete with other invasive species, such as pathogens or other species of plant. Invasive root-feeding weevils could potentially predispose northern forest ecosystems to subsequent biological invasions. For example, several species of invasive plants are known to aggressively colonize forest gaps. Similarly, root-feeding curculionids could potentially predispose stands to invasive earthworms. Our sampling during 2001–2002 indicated low densities of earthworms, only 61 m−2 (R.A. Pinski, 2002, unpublished data), compared to areas in which they have become well established, with densities of >565 m−2 (Eisenhauer et al., 2007). More studies are needed to examine interactions between exotic earthworms and arthropod fauna (Bohlen et al.,

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2004a,b). It is also possible that as earthworms become more established at these sites they could increase activities by established invasive weevils. For example, plants in areas with exotic earthworms have exhibited increased foliage nitrogen levels (Scheu, 2003) – which could increase food quality for adult weevils. Exotic earthworms can decrease fine-root biomass (Fisk et al., 2004), which could negatively impact root-feeding weevil larvae.

8.4. Conclusions A complex of root-feeding weevils is established in North America, ranging throughout south-eastern Canada and the north-eastern USA. Rhizophagous larvae comprise a large portion of the belowground biomass and mesofauna abundance in the northern hardwood forests. They appear to have displaced much of the native fauna. We do not know how they are affecting plant ecology or nutrient cycles, and we have little information regarding their interactions with other native or invasive organisms. Additional research is needed to determine the impacts on ecosystem function, production and overall health.

Acknowledgements We are indebted to the many systematists who provided data for this project: C. Bartlett (University of Delaware), R. Bell (University of Vermont), S. Boucher (McGill University), D. Chandler (University of New Hampshire), G. Fauske (North Dakota State University), C. Freeman (The Ohio State University), P. Johnson (South Dakota State University), S. Krauth (University of Wisconsin), D. Larson (Memorial University), C. Majka (Nova Scotia Museum of Natural History), C. O’Brien (retired, Florida A&M University), G. Parsons (Michigan State University), K. Pickett (University of Vermont), G. Setliff (University of Minnesota), L. Shapiro and K. Kim (Penn State University). This work could not have been completed without the assistance of many dedicated technicians from UW-Madison and the USDA Forest Service. Funding has been provided for this research and publication from the USDA Cooperative State Research, Education and Extension Service (CSREES Proj WI50 and WIS04969), an EPA STAR Fellowship and grant from Applied Ecological Services, Inc., to DRC, and the USDA Forest Service and UW-Madison College of Agriculture and Life Sciences.

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Root Feeders in the Wider Ecosystem

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9

Linking Aboveground and Belowground Herbivory S.N. JOHNSON,1 T.M. BEZEMER2 AND T.H. JONES3 1

Scottish Crop Research Institute, Dundee, UK; 2Netherlands Institute of Ecology (NIOO-KNAW), Heteren, The Netherlands; 3Cardiff University, Cardiff, UK

9.1. Introduction Plants are exploited and attacked by a range of organisms both above and below the soil surface. Many of these interactions play key roles in complex food webs that link aboveground and belowground terrestrial ecosystems (Van der Putten et al., 2001; Wardle et al., 2004). Soil organisms intimately associated with plant roots have the potential to induce marked aboveground effects; these organisms include both mutualists such as mycorrhizal fungi and nitrogen-fixing bacteria, and antagonists such as root pathogens and root herbivores. Of the latter group, insect herbivores are an important component, with increasing attention being focused on how belowground herbivores interact with aboveground herbivores, and vice versa (Masters et al., 1993; Blossey and Hunt-Joshi, 2003). The number of studies investigating interactions between aboveground and belowground insect herbivores remains small. Bezemer et al. (2002) and van Dam et al. (2003), for example, listed only seven and nine studies, respectively, that involved both aboveground and belowground herbivores. Recently however, a growing number of studies (reviewed in Tables 9.1 and 9.2) suggest plant-mediated linkages between root- and foliar-feeding insects are more widespread than previously thought. The earliest studies to examine aboveground–belowground interactions between insect herbivores focussed on paired interactions between insects feeding on shoots and roots (e.g. Gange and Brown, 1989; Masters and Brown, 1992; Masters et al., 1993). This remains the most common type of study. At present, 23 studies have reported the consequences of insect root herbivory for aboveground insect herbivores (Table 9.1), whereas just 13 have reported the reciprocal relationship between aboveground herbivory on root-feeding insects (Table 9.2). This imbalance most likely arises from the difficulty in observing and quantifying the performance of root-feeding insects in the ©CAB International 2008. Root Feeders: An Ecosystem Perspective (eds Johnson and Murray)

153

Aboveground insect herbivore Order

Belowground insect herbivore

Feeding Order guild Reference

Agriotes lineatus

C

CH CH

L. salicaria

C Hylobius transversovittatus H. transversovittatus C

CH

L. salicaria

H. transversovittatus C

CH

Sonchus oleraceus Phyllopertha horticola Food Fragaria × Otiorhynchus consumption ananassa sulcatus Developmental Brassica oleracea Delia radicum rate Size or weight B. oleracea D. radicum gain Developmental B. nigra D. radicum rate Survival B. nigra D. radicum

C

CH

Wurst and Van der Putten (2007) Hunt-Joshi and Blossey (2005) Hunt-Joshi and Blossey (2005) Hunt-Joshi and Blossey (2005) Masters (1992)

C

CH

Gange (2001)

D

CH

Soler et al. (2005)

D

CH

Soler et al. (2005)

D

CH

D

CH

Weight or size gain

D

CH

Van Dam et al. (2005) Van Dam et al. (2005) Van Dam et al. (2005)

Chrysodeixis chalcites Galerucella calmariensis G. calmariensis

L

CH

0

Survival

C

CH

0

C

CH

0

G. calmariensis

C

CH

0

Weight or size gain Population abundance Survival

L Mamestra brassicae C Otiorhynchus sulcatus adults Pieris brassicae L

CH

0

RGR

CH

+

CH

−

P. brassicae

L

CH

0

P. rapae

L

CH

0

P. rapae

L

CH

0

P. rapae

L

CH

−

Plantago lanceolata Lythrum salicaria

B. nigra

D. radicum

S.N. Johnson et al.

Performance parameter changed during Feeding Plant species guild Outcome interaction

154

Table 9.1. Consequences of shoot-feeding insects in reported plant-mediated interactions with root-feeding insects. Order: C = Coleoptera, D = Diptera, H = Homoptera, L = Lepidoptera, ND = not defined; Feeding guild: CH = chewer (mandibulate), SU = sucker (proboscis feeding), ST = stem borer, GA = galler, LM = leaf-miner, SP = seed predator, ND = not defined; Outcome: ‘−’ represents negative impacts on performance, ‘+’ represents positive impacts on performance, ‘0’ represents no significant impacts on performance, RGR = relative growth rate.

L

CH

−

RGR

L

CH

−

S. frugiperda

L

CH

−

Food consumption RGR Oryza sativa

Hayhurstia atriplicis Chromatomyia syngenesiae C. syngenesiae

H

GA

0

D

LM

0

D

LM

0

C. syngenesiae

D

LM

0

C. syngenesiae

D

LM

0

C. syngenesiae

D

LM

0

C. syngenesiae

D

LM

0

C. syngenesiae

D

LM

0

C. syngenesiae

D

LM

0

C. syngenesiae

D

LM

+

C. syngenesiae

D

LM

0

C. syngenesiae

D

LM

+

Stephensia brunnichella

L

LM

−

Population abundance Developmental rate Weight or size gain Developmental rate Weight or size gain Developmental rate Weight or size gain Developmental rate Weight or size gain Weight or size gain Food consumption Weight or size gain Developmental rate

A. lineatus

C

CH

A. lineatus

C

CH

C

CH

Chenopodium album Sonchus arvensis

Lissorhoptrus oryzophilus Pemiphigus betae

H

SU

Agriotes spp.

C

CH

Bezemer et al. (2002) Bezemer et al. (2002) Tindall and Stout (2001) Moran and Whitham (1990) Staley et al. (2008)

S. arvensis

Agriotes spp.

C

CH

Staley et al. (2008)

Sonchus asper

Agriotes spp.

C

CH

Staley et al. (2008)

S. asper

Agriotes spp.

C

CH

Staley et al. (2008)

Sonchus oleraceus Agriotes spp.

C

CH

Staley et al. (2008)

S. oleraceus

Agriotes spp.

C

CH

Staley et al. (2008)

Sonchus palustris

Agriotes spp.

C

CH

Staley et al. (2008)

S. palustris

Agriotes spp.

C

CH

Staley et al. (2008)

S. oleraceus

P. horticola

C

CH

S. oleraceus

P. horticola

C

CH

S. oleraceus

P. horticola

C

CH

Masters and Brown (1992) Masters and Brown (1992) Masters (1995a)

Clinopodium vulgare

Agriotes spp.

C

CH

Staley et al. (2007)

Gossypium herbaceum G. herbaceum

155

Continued

Linking Aboveground and Belowground Herbivory

Spodoptera exigua S. exigua

156

Table 9.1. Continued

Aboveground insect herbivore Order

Performance parameter changed during Feeding Plant species guild Outcome interaction

Belowground insect herbivore

Feeding Order guild Reference

S. brunnichella

L

LM

0

C. vulgare

Agriotes spp.

C

CH

Staley et al. (2007)

C. vulgare

Agriotes spp.

C

CH

Staley et al. (2007)

Asclepias syriaca

Tetraopes tetraophthalmus Agriotes spp.

C

CH

Agrawal (2004)

C

CH

Cardamine pratensis Capsella bursa-pastoris C. bursa-pastoris

Pemphigus populitransversus P. horticola

H

SU

Poveda et al. (2003) Salt et al. (1996)

C

CH

+

Population abundance Weight or size gain Population abundance Population abundance Population abundance Developmental rate Fecundity

S. brunnichella

L

LM

−

Liriomyza asclepiadis Aphids

D

LM

−

H

SU

+

Aphis fabae

H

SU

0

A. fabae

H

SU

0

A. fabae

H

SU

P. horticola

C

CH

A. fabae

H

SU

+

Longevity

C. bursa-pastoris

P. horticola

C

CH

A. fabae

H

SU

+

RGR

C. bursa-pastoris

P. horticola

C

CH

A. fabae

H

SU

+

C. bursa-pastoris

P. horticola

C

CH

Megoura viciae

H

SU

+

SU

0

General root herbivores A. lineatus

ND

H

Ruderal community P. lanceolata

ND

Myzus persicae

C

CH

M. persicae

H

SU

+

S. oleraceus

ND

ND

H H

SU SU

0 +

General root herbivores P. horticola P. horticola

Wurst and Van der Putten (2007) Masters (1995b)

M. persicae M. persicae

Weight or size gain Population abundance Population abundance Population abundance Fecundity RGR

C C

CH CH

Masters (1995b) Masters (1995b)

Sinapis arvensis

S.N. Johnson et al.

S. oleraceus S. oleraceus

Gange and Brown (1989) Gange and Brown (1989) Gange and Brown (1989) Gange and Brown (1989) Gange and Brown (1989) Masters (1992)

SU

+

Terellia ruficauda D

SP

+

General seed ND predators Ostrinia nubilalis L

SP

0

ST

−

General leaf herbivores General leaf herbivores

ND

ND

+

ND

ND

0

Weight or size gain Population abundance Population abundance Population abundance Population abundance Population abundance

C

S. oleraceus

P. horticola

Cirsium palustre Lupine arboreus

General root ND herbivores Hepialus californicus L

Zea mays

Diabrotica spp.

Perennial General root grasses/forbs herbivores Tripleurospermum General root herbivores perforatum

CH

Masters (1995b)

ND

Masters et al. (2001) Maron (1998)

CH

C

CH

ND

ND

ND

ND

White and Andow (2006) Masters et al. (1993) Mullerscharer and Brown (1995)

Linking Aboveground and Belowground Herbivory

H

M. persicae

157

Order

Agriotes lineatus

C

CH

0

RGR

Agriotes spp.

C

CH

0

RGR

Agriotes spp. Agriotes spp.

C C

CH CH

− 0

RGR RGR

Agriotes spp.

C

CH

−

RGR

Agriotes spp.

C

CH

0

RGR

C Hylobius transversovittatus H. transversovittatus C

CH

0

CH

−

Development time Survival

H. transversovittatus C

CH

0

H. transversovittatus C

CH

0

Longitarsus bethae

C

CH

0

L. bethae L. bethae

C C

CH CH

− 0

Weight or size gain Population abundance Development time Survival Weight or size gain

Aboveground insect herbivore

Feeding Order guild Reference

Spodoptera exigua Chromatomyia syngenesiae C. syngenesiae C. syngenesiae

L

CH

D

LM

Bezemer et al. (2003) Staley et al. (2008)

D D

LM LM

Staley et al. (2008) Staley et al. (2008)

Gossypium herbaceum Sonchus arvensis Sonchus asper Sonchus oleraceus Sonchus palustris Clinopodium vulgare Lythrum salicaria L. salicaria

C. syngenesiae

D

LM

Staley et al. (2008)

Stephensia brunnichella Galerucella calmariensis G. calmariensis

L

LM

Staley et al. (2008)

C

CH

C

CH

L. salicaria

G. calmariensis

C

CH

L. salicaria

G. calmariensis

C

CH

H

SU

Hunt-Joshi and Blossey (2005) Hunt-Joshi and Blossey (2005) Hunt-Joshi and Blossey (2005) Hunt-Joshi and Blossey (2005) Simelane (2006)

H H

SU SU

Simelane (2006) Simelane (2006)

Lantana camara Teleonemia scrupulosa L. camara T. scrupulosa L. camara T. scrupulosa

S.N. Johnson et al.

Belowground insect herbivore

Performance parameter changed during Feeding Plant species guild Outcome interaction

158

Table 9.2. Consequences for root-feeding insects in reported plant-mediated interactions with shoot-feeding insects. Order: C = Coleoptera, D = Diptera, H = Homoptera, ND = not defined; Feeding guild: CH = chewer (mandibulate), SU = sucker (proboscis feeding), ND = not defined; Outcome: ‘−’ represents negative impacts on performance, ‘+’ represents positive impacts on performance, ‘0’ represents no significant impacts on performance, RGR = relative growth rate.

C

CH

−

Phyllopertha horticola P. horticola

C

CH

−

C

CH

0

Delia radicum

D

SU

0

D. radicum D. radicum

D D

SU SU

− −

Lissorhoptrus oryzophilus L. oryzophilus

H

SU

−

H

SU

−

Pemiphigus betae

H

SU

−

P. betae

H

SU

−

Pemphigus populitransversus General root herbivores

H

SU

−

ND

ND

−

Population abundance RGR

L. camara

T. scrupulosa

H

SU

Simelane (2006)

S. oleraceus

C. syngenesiae

D

LM

Weight or size gain Development time Survival Weight or size gain Population abundance Weight or size gain Population abundance Weight or size gain Population abundance Population abundance

S. oleraceus

C. syngenesiae

D

LM

Masters (1992, 1995b) Masters (1992)

B. nigra

Pieris brassicae

C

CH

Soler et al. (2007)

B. nigra B. nigra

P. brassicae P. brassicae

C C

CH CH

Soler et al. (2007) Soler et al. (2007)

Oryza sativa

S. frugiperda

L

CH

O. sativa

S. frugiperda

L

CH

Chenopodium album C. album

Hayhurstia atriplicis H. atriplicis

H

GA

H

GA

Cardamine pratensis Perrenial grasses/forbs

Aphis fabae

H

SU

Tindall and Stout (2001) Tindall and Stout (2001) Moran and Whitham (1990) Moran and Whitham (1990) Salt et al. (1996)

General leaf herbivores

ND

ND

Masters et al. (1993)

Linking Aboveground and Belowground Herbivory

L. bethae

159

S.N. Johnson et al.

160

soil, and this remains a significant challenge for studying aboveground– belowground interactions in any detail (Johnson et al., 2007). In this respect, there is an inevitable bias towards studies of the effects of root-feeding insects on foliar-feeding insects, with far fewer investigations of the reverse, which is also reflected in this chapter. The aim of this chapter is to review existing examples of plant-mediated interactions between aboveground and belowground insect herbivores, and explore the mechanisms underpinning such interactions, with particular emphasis on how root-feeding insects change host plants in a manner that potentially affects aboveground communities. We raise the issue of how trophic complexity is increasingly becoming central to our understanding of aboveground–belowground interactions, and attempt to identify future questions for research. In this chapter, we focus solely on the interactions between root-feeding and foliar-feeding insect herbivores because the role of nematode root herbivory in aboveground–belowground interactions has been reviewed elsewhere (e.g. Mortimer et al., 1999).

9.2. Impacts of Root-feeding Insects on Aboveground Insect Herbivores 9.2.1. Examples in the literature and current trends Masters et al. (1993) were the first to propose a conceptual model for interactions between aboveground and belowground herbivores. They based their model on the modest number of studies that were available at the time and concluded that aboveground insect herbivores tended to benefit from root herbivory (see Table 9.1), resulting in increased fecundity (Masters, 1992), prolonged longevity (Gange and Brown, 1989), faster growth rates (Masters, 1995a), increased weight gain (Masters and Brown, 1992) and greater population increase (Moran and Whitham, 1990). Basing their model on the plant-stress hypothesis (White, 1984), Masters et al. (1993) proposed a mechanism for these positive effects due to impairment of root function by root herbivory. Prolonged water stress impairs protein metabolism and amino acid synthesis in plants (Brodbeck and Strong, 1987), which is frequently associated with the hydrolysis of existing proteins to free amino acids in the foliage (see the more recent review by Huberty and Denno, 2004). Because nitrogen is generally limiting for many insect herbivores, water stress can therefore result in improved insect herbivore performance (White, 1969). Masters et al. (1993) proposed that root herbivory impairs the plant’s ability to take up water and nutrients from the soil, resulting in a reduction in the relative water content of foliage and an increase in soluble nitrogen (e.g. amino acids) and carbohydrates, which potentially promotes insect performance. This conceptual model was elaborated on by Bezemer et al. (2002) and termed the ‘stress response hypothesis’. Foliar-feeding aphids, in particular, which directly feed on the phloem, respond to root herbivory as predicted from the stress response hypothesis

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161

(Table 9.1). Five of the six studies report positive effects of root herbivory on aphid performance. In one of the studies reporting no significant effect of root herbivory on aphid performance (Salt et al., 1996), the root herbivore was a sap-sucking aphid rather than a chewing insect as in the other studies (Gange and Brown, 1989; Masters, 1995a; Masters et al., 2001; Poveda et al., 2003; Wurst and Van der Putten, 2007). Phloem-feeding and chewing herbivores differ in the type and amount of damage they cause to their host plant, and plant responses to this damage can be distinctly different (Bezemer and Van Dam, 2005). This may explain the observed differences in responses of foliar-feeding aphids to the two types of root herbivory. As an alternative mechanism, Bezemer et al. (2002) also proposed the ‘defence induction hypothesis’, which predicted that root herbivory can affect aboveground herbivores detrimentally through the systemic induction of foliar plant defence compounds (allelochemicals). Plants produce a variety of chemical defence compounds, which often increase following herbivore attack (Karban and Baldwin, 1997). Plant hormones, such as jasmonic, salicylic and abscisic acids, and ethylene that have important roles in determining induced defence responses in plants are transported within the plant via the vascular system, which connects aboveground and belowground plant tissues. Induced plant responses can therefore occur both locally at the site of attack, and systemically in other, undamaged, parts of the plant. Although plant defence induction has been studied primarily in an aboveground context (Bezemer and Van Dam, 2005), plant defence compounds are also found in root tissues. A number of compounds produced in the roots are also expressed in the foliage (Van Dam et al., 2003). The defence induction hypothesis (see Bezemer et al., 2002) states that root herbivory causes systemic induction of plant defence compounds in the foliage, leading to reduced performance of aboveground herbivores. For example, root feeding by wireworms, Agriotes lineatus L. (Coleoptera: Elateridae), can cause a 50% increase in terpenoids in cotton (Gossypium herbaceum L.) leaves, negatively affecting beet armyworm larvae, Spodoptera exigua Hübner (Lepidoptera: Noctuidae), feeding on the foliage, with development rates decreasing by approximately 50% (Bezemer et al., 2003). Several other studies have reported that plant defence compounds in foliage increase following root herbivory (e.g. Bezemer et al., 2004; Soler et al., 2005; Van Dam et al., 2005) although exposure to root herbivory by nematodes, for example, can also lead to significant decreases in defence compounds such as nicotine, phenolics or glucosinolates (Hanounik and Osborne, 1977; Bezemer and Van Dam, 2005; Van Dam et al., 2005). Further support of the defence induction hypothesis comes from other studies reporting reduced aboveground insect growth rates (Soler et al., 2005), retarded growth rates (Tindall and Stout, 2001) and reduced weight gain (Van Dam et al., 2005). Aboveground insect herbivores show a variety of responses to root herbivore-induced changes in the shared host plant (Table 9.1), with the mode of aboveground feeding influencing the response to root herbivory. Three feeding groups are relatively well studied: leaf-chewing insects are generally negatively influenced by root herbivory (five negative responses, eight examples of no effects and one positive response); leaf-mining insects

162

S.N. Johnson et al.

are largely unaffected (three negative responses, ten studies reported no effect and two reported positive responses); and phloem feeders generally respond positively to root herbivory (four examples of no reported effects and ten positive responses). A recent meta-analysis of the effects of water stress on insect performance showed that water stress generally does not influence leaf-chewing insects, while aphid species tend to benefit from host plant water stress, particularly so when this is intermittent (Huberty and Denno, 2004). Sap-sucking insects could therefore benefit from increased levels of soluble nitrogen, but circumvent the effects of induced defensive compounds since they frequently occur in very low concentrations in the phloem (Raven, 1983; Karban and Myers, 1989). In contrast, chewing insects may be more susceptible to induced defensive compounds in the leaves, even when nutritional quality is increased. Despite this tentative generalization about the mode of feeding of aboveground insect herbivores, it should also be noted that in the context of aboveground– belowground interactions, individual species within feeding guilds often show different and opposing effects to root herbivory (see Table 9.1).

9.2.2. How do root-feeding insects change host plant quantity and quality? Both the nutrient stress (Masters et al., 1993) and defence induction (Bezemer et al., 2002) hypotheses are supported by different studies, although it should be noted that they are not mutually exclusive. It is obvious that root-feeding insects can influence aboveground plant growth and nutritional quality in a variety of ways (Blossey and Hunt-Joshi, 2003), and aboveground insect herbivores show a range of responses to such changes in their host plant (Schoonhoven et al., 2005). For a mechanistic understanding of how root herbivory will influence aboveground herbivores it is essential to understand the effects that root herbivory can have on the host plant. These effects can be broadly grouped into three categories: effects on plant growth, on plant phenology and on plant nutritional quality. Many studies that have measured the effect of root herbivory on plant growth show a reduction in aboveground plant vegetative or reproductive biomass, plant height or variables such as number of leaves or seeds (e.g. Gange, 2001; Dawson et al., 2002; Borowicz et al., 2005). This has been explained by compensatory root growth at the cost of shoot growth or via reduced nutrient or water uptake of the root system (Andersen, 1987; Brown and Gange, 1990). Root herbivory, however, does not always lead to a reduction in aboveground plant growth (e.g. Bezemer et al., 2003; Soler et al., 2005), and the impact of root herbivory may depend on other variables such as nutrient or water availability that limit plant growth (Wise and Abrahamson, 2005). Changes in plant quality will, most likely, influence herbivore population abundance more than individual growth parameters as most plant species are not completely defoliated by one individual insect herbivore. Although root herbivory may also lead to phenological changes in the host plant, for example, onset of flowering, flowering duration or senescence,

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163

the few studies that have measured plant phenology generally show that this is not the case (e.g. Moron Rios et al., 1997; Nötzold et al., 1998; Poveda et al., 2003, 2005). This dearth of evidence may be the result of most studies considering the effects of root herbivory on the host plant and aboveground herbivory for relatively short periods of time (days or weeks rather than months). Phenological changes, if they occur, could alter the temporal availability of the host plant for insect herbivores and influence population abundance and related parameters. As discussed briefly above, root herbivory can cause a range of physiological changes in plants, directly affecting nutritional quality of aboveground herbivores. Reported effects include changes in water content, nitrogen, carbohydrates (Masters et al., 1993; Blossey and Hunt-Joshi, 2003) and allelochemicals (Bezemer and Van Dam, 2005), and also in foliar minerals such as potassium, phosphorus and other micro-elements (e.g. Coale and Cherry, 1989; Borowicz et al., 2005). As root herbivory can affect photosynthesis directly (e.g. Riedell, 1990; Godfrey et al., 1993; Murray et al., 2002), changes in plant nutritional quality in response to root herbivory can be the result of a number of different changes in the host plant, for example, changes in allocation, induced plant defence responses, or changes in plant growth or nutritional uptake. Any changes in plant tissue nutritional quality can directly influence insect performance.

9.3. Impacts of Aboveground Insect Herbivores on Root-feeding Insects There are comparatively few examples of how aboveground insects affect root-feeding insects (Table 9.2), which inevitably limits discussion here on this aspect of linkages between aboveground and belowground herbivores. The potential mechanisms underpinning such interactions are even less clear. There are currently no examples of root-feeding insects benefiting from aboveground herbivory, with 56% of the impacts on root herbivore performance being detrimental in the form of slower growth rates (Salt et al., 1996) or reduced survival (Soler et al., 2007a), weight gain (Tindall and Stout, 2001) and population growth (Moran and Whitham, 1990). Foliar herbivory causes a shift in source–sink relationships within the plant (Masters et al., 1993; Masters and Brown, 1997), whereby resources are committed aboveground and root biomass decreases. The reduced root biomass is thought to underpin the detrimental impacts on root-feeding insects. While some studies support this hypothesis (e.g. Moran and Whitham, 1990) others, such as Soler et al. (2007a), reported no overall reduction in root biomass, but significant increases in root indole glucosinolates (up to 50% higher) following foliar herbivory. This seems a more plausible mechanism for the negative interaction (see Table 9.2). Relatively few studies have addressed such defence responses in root tissues following aboveground herbivory. However, other studies also show that foliar herbivory or surrogates for aboveground herbivory such as the application of the hormones jasmonic or salicylic acid to

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leaves can lead to an increase in plant defence compounds in roots (e.g. Ludwig-Muller et al., 1997; Van Dam et al., 2005). The opposite effect has also been shown. In Ragwort (Senecio jacobaea L.), for example, alkaloid concentrations were lower in roots of plants exposed to aboveground herbivory than in control plants (Hol et al., 2004). Interpreting the impacts of aboveground insect herbivores on root feeders is more challenging than vice versa as much less is known about how the nutritional and defensive chemistry in the roots affects root-feeding insects (Rasmann and Agrawal, 2008). Blossey and Hunt-Joshi (2003), however, made a convincing argument based on indirect evidence that root herbivores are stronger competitors than aboveground insects, particularly in later successional plant communities. In particular, they speculate that the longer larval life cycle of root herbivores results in later successional plants already having been challenged before folivores arrive (unlike many experiments that simultaneously subject the plant to both root and foliar feeders).

9.4. New Topics and Future Prospects for Linking Aboveground and Belowground Herbivory 9.4.1. Incorporating trophic complexity So far, all studies discussed in this chapter have focused on paired combinations of aboveground and belowground insect herbivores. More recent studies have begun to address more complex interactions involving other trophic groups. In particular, several studies have investigated that higher trophic groups occurring aboveground are indirectly affected by root herbivory. Wackers and Bezemer (2003), for example, demonstrated that root herbivory by wireworms (A. lineatus) increased extrafloral nectar production in cotton plants (G. herbaceum). This is known to attract predators of aboveground insect herbivores. Further studies by Poveda et al. (2003, 2007) expanded this investigation to include two further aboveground insects (a pollinator and an aphid parasitoid) and report a beneficial impact on both groups following root herbivory. Root herbivory by the cabbage root fly, Delia radicum L. (Diptera: Anthomyiidae), via a reduction in aboveground nutritional quality of the host plant black mustard (Brassica nigra L.), negatively influenced the caterpillar Pieris brassicae L. (Diptera: Pieridae) which feeds from the foliage. This, in turn, negatively affected the performance of the parasitoid Cotesia glomerata L. (Hymenoptera: Braconidae) developing in P. brassicae and, subsequently the hyper parasitoid Lysibia nana, which developed in C. glomerata (Soler et al., 2005). Root herbivory thus influenced a four-trophic-level aboveground food chain. More recently, Soler et al. (2007c) provided evidence that root herbivory by D. radicum also influenced the aboveground volatile blend emitted by black mustard. Furthermore, the volatile blend emitted by the plant in response to root herbivory differed distinctly from the blend emitted following aboveground herbivory. Many plants produce and release plant volatile compounds

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165

in response to herbivore feeding, and these volatiles can be used by natural enemies such as predators or parasitoids of the attacking herbivores to locate their hosts (Vet and Dicke, 1992). All these studies illustrate how the effects of root herbivory surpass the effects on plant nutritional quality and herbivore performance. Root herbivores have the potential to influence searching behaviour of herbivores and organisms of higher trophic levels and thus alter aboveground community composition. Recent work has also shown that similar tritrophic effects may occur belowground. Roots of plants exposed to root herbivores can excrete compounds into the soil that result in attraction of entomopathogenic nematodes, which are important natural enemies of root-feeding insects (Van Tol et al., 2001; Rasmann et al., 2005; Rasmann and Turlings, 2007). The compounds involved in these tritrophic interactions can be identical to the compounds involved in aboveground interactions (Rasmann et al., 2005; Rasmann and Turlings, 2007). Whether aboveground herbivory can influence excretion of these compounds into the soil, and hence influence root herbivores via influencing the natural enemies of the root herbivores, is an important question that remains to be more fully explored. This chapter concentrates on the interactions between root-feeding and aboveground insect herbivores; however, root herbivores are only a component, albeit integral, part of the soil ecosystem (Jones and Bradford, 2001; Bardgett, 2005). Root feeders interact with, and are affected by, various microbial and pathogenic organisms and so habitat quality, and therefore herbivore success, is defined and influenced by comminutors (e.g. Collembola) and ecological engineers (e.g. earthworms). An improved understanding of the linkages between the aboveground and belowground subsystems, and their consequences on ecosystem function, requires a detailed understanding of the interactions that occur in soil food webs and how these regulate nutrient availability.

9.4.2. From laboratory to the field Studying aboveground–belowground herbivore interactions under realistic conditions is difficult. Many of the examples cited above are derived from studies conducted with early successional plant species (e.g. Moran and Whitham, 1990; Masters, 1995b; Ganade and Brown, 1997), using late-instar generalist root feeders (e.g. Gange and Brown, 1989), frequently over short periods of time (e.g. Masters, 1995a). In the case of field studies, many investigations used plants that colonized bare or tilled ground (Masters et al., 1993). Moreover, some studies used artificial damage to roots to simulate herbivory, largely for pragmatic reasons (Blossey and Hunt-Joshi, 2003). Issues related to artificial (simulated) herbivory in aboveground–belowground interactions were reviewed extensively by Blossey and Hunt-Joshi (2003). They concluded that mechanical root damage caused significantly greater limitation on root ability to maintain adequate water supply to aerial parts of the plant (e.g. Riedell, 1990) and that root volume, CO2 assimilation,

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leaf stomatal conductance and the volume of adventitious roots were significantly different in treatments where maize plants were damaged using artificial herbivory compared to treatments using natural herbivory by Diabrotica spp. (Riedell and Reese, 1999). Blossey and Hunt-Joshi (2003) also highlighted how both aboveground- and belowground-feeding herbivores may result in volatile emissions that attract natural enemies. Various studies (e.g. Kost and Heil, 2006; Puntieri et al., 2006) indicate that artificial herbivory does not elicit such responses.

9.5. Conclusions Studies of the linkages between aboveground and belowground herbivory are limited, but have gathered pace in the last few years with particular developments in the area of induced defensive chemistry. There now seem to be some emerging patterns from the paired interaction studies reported so far, with aboveground phloem feeders generally benefiting from root herbivory, whereas chewing folivores tend to be adversely affected. Apart from the rudimentary measurements (e.g. total soluble nitrogen) made by the earliest studies (Gange and Brown, 1989), little progress has been made towards characterizing nutritional mechanisms underpinning aboveground–belowground interactions. For instance, significant changes in the mineral and micro-element concentrations of leaves are known to occur in response to root herbivory (Coale and Cherry, 1989; Borowicz et al., 2005) yet their impacts aboveground have not been fully investigated. The introduction of trophic complexity into model systems is an important and emerging area of research that is likely to increase. A significant challenge will be to incorporate issues such as the influence of global climate change on aboveground–belowground linkages (see Staley and Johnson, Chapter 11, this volume), and to address the important question of how to relate short-term experimental observations to realistic field circumstances, for both natural and managed ecosystems.

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interactions via induced plant defenses. Trends in Ecology and Evolution 20, 617–624. Bezemer, T.M., Wagenaar, R., van Dam, N.M. and Wackers, F.L. (2002) Interactions between root and shoot feeding insects mediated by primary and secondary plant compounds. Proceedings of the Section Experimental and Applied Entomology of the Netherlands Entomological Society (NEV) 13, 117–121. Bezemer, T.M., Wagenaar, R., Van Dam, N.M. and Wackers, F.L. (2003) Interactions

Linking Aboveground and Belowground Herbivory between above- and belowground insect herbivores as mediated by the plant defense system. Oikos 101, 555–562. Bezemer, T.M., Wagenaar, R., Van Dam, N.M., Van Der Putten, W.H. and Wackers, F.L. (2004) Above- and below-ground terpenoid aldehyde induction in cotton, Gossypium herbaceum, following root and leaf injury. Journal of Chemical Ecology 30, 53–67. Blossey, B. and Hunt-Joshi, T.R. (2003) Belowground herbivory by insects: influence on plants and aboveground herbivores. Annual Review of Entomology 48, 521–547. Borowicz, V.A., Alessandro, R., Albrecht, U. and Mayer, R.T. (2005) Effects of nutrient supply and below-ground herbivory by Diaprepes abbreviatus L. (Coleoptera: Curculionidae) on citrus growth and mineral content. Applied Soil Ecology 28, 113–124. Brodbeck, B. and Strong, D. (1987) Amino acid nutrition of herbivorous insects and stress to host plants. In: Barbosa, P. and Schultz, J.C. (eds) Insect Outbreaks: Ecological and Evolutionary Perspectives. Academic Press, New York, pp. 347–364. Brown, V.K. and Gange, A.C. (1990) Insect herbivory below ground. Advances in Ecological Research 20, 1–58. Coale, F.J. and Cherry, R.H. (1989) Impact of White Grub (Ligyrus subtropicus Blatchley) infestation on sugarcane nutrition. Journal of Plant Nutrition 12, 1351–1359. Dawson, L.A., Grayston, S.J., Murray, P.J. and Pratt, S.M. (2002) Root feeding behaviour of Tipula paludosa (Meig.) (Diptera: Tipulidae) on Lolium perenne L. and Trifolium repens L. Soil Biology and Biochemistry 34, 609–615. Ganade, G. and Brown, V.K. (1997) Effects of below-ground insects, mycorrhizal fungi and soil fertility on the establishment of Vicia in grassland communities. Oecologia 109, 374–381. Gange, A.C. (2001) Species-specific responses of a root- and shoot-feeding insect to arbuscular mycorrhizal colonization of its host plant. New Phytologist 150, 611–618. Gange, A.C. and Brown, V.K. (1989) Effects of root herbivory by an insect on a foliar-

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S.N. Johnson et al. Brown, V.K. and Drent, R.H. (eds) Herbivores: Between Plants and Predators. Blackwell Science, Oxford, pp. 205–238. Müller-Schärer, H. and Brown, V.K. (1995) Direct and indirect effects of above-ground and below-ground insect herbivory on plant-density and performance of Tripleurospermum perforatum during early plant succession. Oikos 72, 36–41. Murray, P.J., Dawson, L.A. and Grayston, S.J. (2002) Influence of root herbivory on growth response and carbon assimilation by white clover plants. Applied Soil Ecology 20, 97–105. Nötzold, R., Blossey, B. and Newton, E. (1998) The influence of below ground herbivory and plant competition on growth and biomass allocation of purple loosestrife. Oecologia 113, 82–93. Poveda, K., Steffan-Dewenter, I., Scheu, S. and Tscharntke, T. (2003) Effects of belowand above-ground herbivores on plant growth, flower visitation and seed set. Oecologia 135, 601–605. Poveda, K., Steffan-Dewenter, I., Scheu, S. and Tscharntke, T. (2005) Floral trait expression and plant fitness in response to below- and aboveground plant–animal interactions. Perspectives in Plant Ecology Evolution and Systematics 7, 77–83. Poveda, K., Steffan-Dewenter, I., Scheu, S. and Tscharntke, T. (2007) Plant-mediated interactions between below- and aboveground processes: decomposition, herbivory, parasitism and pollination. In: Ohgushi, T., Craig, T.P. and Price, P.W. (eds) Ecological Communities: Plant Mediation in Indirect Interactions. Cambridge University Press, Cambridge, pp. 147–163. Puntieri, J.G., Stecconi, M., Brion, C., Mazzini, C. and Grosfeld, J. (2006) Effects of artificial damage on the branching pattern of Nothofagus dombeyi (Nothofagaceae). Annals of Forest Science 63, 101–110. Rasmann, S. and Turlings, T.C.J. (2007) Simultaneous feeding by aboveground and belowground herbivores attenuates plant-mediated attraction of their respective natural enemies. Ecology Letters 10, 926–936.

Linking Aboveground and Belowground Herbivory Rasmann, S. and Agrawal, A.A. (2008) In defense of roots: a research agenda for studying plant resistance to belowground herbivory. Plant Physiology 146, 875–880. Rasmann, S., Köllner, T.G., Degenhardt, J., Hiltpold, I., Toepfer, S., Kuhlmann, U., Gershenzen, J. and Turlings, T.C.J. (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434, 732–737. Raven, J.A. (1983) Phytophages of xylem and phloem – a comparison of animal and plant sap-feeders. Advances in Ecological Research 13, 135–234. Riedell, W.E. (1990) Rootworm and mechanical damage effects on root morphology and water relations in maize. Crop Science 30, 628–631. Riedell, W.E. and Reese, R.N. (1999) Maize morphology and shoot CO2 assimilation after root damage by western corn rootworm larvae. Crop Science 39, 1332–1340. Salt, D.T., Fenwick, P. and Whittaker, J.B. (1996) Interspecific herbivore interactions in a high CO2 environment: root and shoot aphids feeding on Cardamine. Oikos 77, 326–330. Schoonhoven, L.M., van Loon, J.J.A. and Dicke, M. (2005) Insect–Plant Biology, 1st edn. Oxford University Press, Oxford. Simelane, D.O. (2006) Effect of herbivory by Teleonemia scrupulosa on the performance of Longitarsus bethae on their shared host, Lantana camara. Biological Control 39, 385–391. Soler, R., Bezemer, T.M., Van der Putten, W. H., Vet, L.E.M. and Harvey, J.A. (2005) Root herbivore effects on above-ground herbivore, parasitoid and hyperparasitoid performance via changes in plant quality. Journal of Animal Ecology 74, 1121–1130. Soler, R., Bezemer, T.M., Cortesero, A.M., Van der Putten, W.H., Vet, L.E.M. and Harvey, J.A. (2007a) Impact of foliar herbivory on the development of a rootfeeding insect and its parasitoid. Oecologia 152, 257–264. Soler, R., Harvey, J.A. and Bezemer, T.M. (2007b) Foraging efficiency of a parasitoid of a leaf herbivore is influenced by root

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10

Root Feeders in Heterogeneous Systems: Foraging Responses and Trophic Interactions

G.N. STEVENS,1 K.O. SPENCE2 AND E.E. LEWIS2 1

College of Natural Sciences and Mathematics, Ferrum College, Ferrum, VA, USA; 2University of California, Davis, CA, USA

10.1. Introduction Root herbivores occupy the ‘middle management’ position in soil food webs. They are dependent on root production, but are also controlled to varying degrees by natural enemies such as entomopathogenic nematodes (EPNs) and fungi, which in turn have their own suite of antagonists that influence the prevalence of top-down control. Abiotic heterogeneity, the well-recognized variability in soil resources and conditions within ecosystems, has direct influences on each of these trophic levels (Hunter and Price, 1992). In addition, this heterogeneity may regulate the stability of interactions between predators and their prey (Hilborn, 1975; Murdoch, 1977) by either reducing natural enemy dispersal rates and thereby providing temporary refuges from predation (e.g. Brockhurst et al., 2006), or through the development of enemyfree spatial refuges (e.g. Schrag and Mittler, 1996). Examples of the effects of heterogeneity on root herbivory within ecosystems demonstrate complex, and often indirect, linkages. One such example occurs in the coastal California bush lupine – ghost moth – EPN system: periodic diebacks of several thousand mature bush lupine (Lupinus arboreus Sims) at various locations within the Bodega Marine Reserve are caused by the root-boring ghost moth, Hepialus californicus Boisduval (Lepidoptera: Hepialidae) (Strong et al., 1995, 1996, 1999). The effects of the root-feeding ghost moth are highly heterogeneous in time: interannual variability in El Niño Southern Oscillation cycles influence rainfall patterns at the reserve, which in turn influences the tendency of native populations of the EPN, Heterorhabditis marelatus Liu (Rhabditida: Heterorhabditidae), to control ghost moths and prevent lupine dieback (Preisser and Strong, 2004). In addition to this strong temporal pattern, fine-scale spatial heterogeneity in soil moisture content plays a significant role in this trophic cascade. Soils close to lupine roots often remain moist when rainfall ceases during the summer months; ©CAB International 2008. Root Feeders: An Ecosystem Perspective (eds Johnson and Murray)

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this moisture facilitates the survival of H. marelatus in the lupine rhizosphere and thereby protects the lupines from root herbivory (Preisser et al., 2006). Another example of the strong effect of heterogeneity on multitrophic interactions involving root herbivores can be found in Florida, where regulation of the citrus root weevil, Diaprepes abbreviatus L. (Coleoptera: Curculionidae), by native and applied EPNs (see Goldson and Gerard, Chapter 7, this volume) appears to be strongly influenced by large-scale variability in soil texture. In this case, the coarse sand content of orchard soils is positively associated with the prevalence of native nematodes such as Steinernema diaprepesi Nguyen and Duncan (Rhabditida: Steinernematidae), and is also positively correlated with the effectiveness of biological control of the citrus root weevil by either native or applied nematodes (McCoy et al., 2002; Duncan et al., 2003). Improving our understanding of root herbivores in ecosystems requires considering both the role of heterogeneity and the effects of natural enemies. In this chapter, we will highlight a range of disparate studies to examine how plants, root herbivores and their natural enemies interact in the complex soil environment. Heterogeneity influences the foraging behaviour of plant roots, as well as the foraging behaviour of root-feeding insects and a key group of their natural enemies, EPNs (Stevens et al., 2007a). Plant-parasitic nematodes such as Meloidogyne incognita (Kofoid and White) Chitwood (Tylenchida: Heteroderidae) also exhibit strong responses to soil cues; interestingly, EPNs can have strong, although indirect, influences on these root-feeding nematodes as well. Within this review, we will focus on these interactions among plants, root feeders and nematodes principally at the sub-metre scale, the approximate range of heterogeneity that is perceived by a larval insect root feeder, plant root or nematode. We will begin by refining our definition of resource heterogeneity for the purpose of this review.

10.2. Resource Heterogeneity Nutrient distributions in the soil exhibit considerable patchiness, typically referred to as heterogeneity. Many different variables lead to the development of soil heterogeneity, including inputs of plant litter, frass, the bodies of decomposing animals and mineral fertilizer (Hodge, 2006). This heterogeneity has been characterized in a range of ecosystems, including forests (Gonzalez and Zak, 1994; Gross et al., 1995; Farley and Fitter, 1999; Lister et al., 2000), deserts (Schlesinger et al., 1996) and agricultural fields (Robertson et al., 1997). Research conducted at the Kellogg Biological Station (Michigan, USA) found both significant heterogeneity and strong associations between the availability of soil resources, the activity of soil microbes and plant productivity (Robertson et al., 1997), even within a field that had been cultivated annually for more than a century. Significant heterogeneity in nutrient availability and bacterial activity is seen at the sub-metre scale, well within the rooting zone of an individual plant or the foraging zone of a root herbivore (Stoyan et al., 2000; Nunan et al., 2002).

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This heterogeneity can have significant influences on plant communities (Robinson et al., 1999; Bliss et al., 2002); in turn, the plants themselves can also be strong drivers of resource patterns within ecosystems (Guo et al., 2004). Root herbivores may respond to soil heterogeneity directly via foraging behaviour (see below), but they also respond to the heterogeneity of their preferred food source and are influenced by the spatial and temporal distributions of their natural enemies. Underlying patterns of soil resources can have strong effects on trophic interactions (Hunter and Price, 1992; Karr et al., 1992), and the response of plants, root herbivores and their natural enemies to this heterogeneity is a key component of soil food web structure and function.

10.3. The Response of Plants to Heterogeneity It is the root systems of plants that respond to soil nutrient heterogeneity. The amount of photosynthesis allocated to root systems is influenced by a range of variables; the general rule of thumb, though, is that between onethird and two-thirds of the carbon a plant fixes via photosynthesis is allocated to root production and maintenance, including the production of root exudates and mycorrhizae (Jackson et al., 1997; Matamala et al., 2003). Root responses to soil heterogeneity are relevant both as the base of root herbivore food webs and also from the perspective of carbon and nutrient cycling within soil systems. Research conducted by Drew and colleagues on barley (Hordeum vulgare L.) root responses to bands of soil fertilizer in the 1970s might be considered a touchstone for research on plant responses to soil heterogeneity. Drew and colleagues analysed barley rooting behaviour, comparing root production patterns in uniformly fertilized sands to patterns produced when one of the key macronutrients (N, P or K) was concentrated in horizontal bands approximately 10 cm below the soil surface. Patches of nitrate, ammonium or phosphorus fertilizer led to a two- to threefold stimulation of root production within the fertilized band, while potassium fertilizer did not result in a response (Drew et al., 1973; Drew, 1975; Drew and Saker, 1975). Many species of plant demonstrate significant plasticity in response to soil heterogeneity. Plants may alter rates of nutrient uptake, demography, morphology or mycorrhizal colonization in response to nutrient-rich soil patches (Fitter, 1987, 1994; Hutchings, 1988; Jackson et al., 1990; Allen, 1992; Pregitzer et al., 1993; Duke et al., 1994; Robinson, 1994; Smith et al., 1997). These responses may be optimized for individual spatio-temporal patterns of heterogeneity (Hutchings, 1988; Campbell et al., 1991; Hutchings and Dekroon, 1994; Eissenstat and Yanai, 1997; Wijesinghe et al., 2001), and the result of these nutrient-foraging decisions may have significant ramifications for total nutrient uptake and whole-plant carbon gain (Nye and Tinker, 1977; Caldwell et al., 1992; Robinson, 1994; Gleeson and Fry, 1997; Huber-Sannwald et al., 1998; Fransen et al., 2001). Root proliferation responses to soil heterogeneity may be an important component of interactions with root herbivores. Plant roots generally

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proliferate in nutrient-rich patches, although this response may vary significantly even between species within the same plant community (Campbell et al., 1991; Einsmann et al., 1999; Farley and Fitter, 1999; Bliss et al., 2002; Rajaniemi and Reynolds, 2004). Studies such as these that have examined the range of foraging responses observed across a plant community have shown differences among species both in terms of morphological precision (i.e. the tendency to proliferate roots in nutrient-rich patches) as well as sensitivity to patches (measured as an increase in whole-plant growth as nutrient heterogeneity increases). This variability among species in the strength and nature of the root-foraging response is thought to be an important component of competition in plant communities (Robinson et al., 1999; Casper et al., 2000; Fransen and De Kroon, 2001; Bliss et al., 2002). This significant variation among species also points to potential tradeoffs for root-foraging behaviours. A plant may benefit from precisely foraging for soil nutrients and increase the amount of nutrients it is able to capture by increasing the efficiency of nutrient capture, that is the grams of nutrients obtained per gram of root tissue produced (Eissenstat and Yanai, 1997), or by the ability to co-opt resources from competitors (Robinson, 1994; Hodge et al., 1999). However, these benefits must be balanced by the costs involved in foraging. The most obvious of these is the cost of root tissue production and maintenance; other potential costs include exposure to abiotic stresses such as drought or flooding (Jansen et al., 2005; Neatrour, 2005), as well as biotic stressors such as root herbivory (Stevens and Jones, 2006a,b). If both roots and root herbivores are attracted to nutrient-rich patches, roots in fertile patches may be more vulnerable to herbivory than roots in areas with reduced fertility (Stevens and Jones, 2006a; Stevens et al., 2007a).

10.4. Heterogeneity and Root Herbivores Root herbivory results in removal of a significant proportion of the plant biomass used for root construction. Although we find root herbivores in a wide range of ecosystems, we often lack information on the amount of root herbivory that actually occurs, the spatial variation in root herbivory within ecosystems, as well as the influence of root herbivory on carbon and nutrient cycles. We do know that root herbivores can influence the composition of plant communities through effects on the performance of individual plants as well as influences on competitive interactions among plant species (Brown and Gange, 1990; Brussaard, 1998; Coffin et al., 1998). An often-observed effect of root herbivores on plant communities has been a growth reduction of dominant species or individuals within the community (Brown and Gange, 1990; van Ruijven et al., 2005). These effects can be strong, particularly in agricultural systems, where their effects are often more readily observed through mortality or reduced yield. In the fruit- and nut-growing regions of the California Central Valley, the Ten-lined June beetle, Polyphylla decemlineata Say (Coleoptera: Scarabaeidae), has been implicated in periodic, extensive dieback of almond, apple and

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walnut trees (Johnson et al., 2003). Citrus-growing regions in Florida have been dramatically altered after the invasion of the root-feeding citrus root weevil, D. abbreviatus, an insect native to the Caribbean. D. abbreviatus has become one of the key insect pests in the Florida citrus industry (DTF, 1997). More recently, populations of D. abbreviatus have been found at multiple sites within southern California, leading to an extensive eradication effort (Flores, 2007), as well as a search for suitable natural enemies already present in the state. In addition to the direct damage from root herbivory, root-feeding insects can create optimum conditions for establishment of root pathogens such as Phytophthora spp. The symptoms of root herbivory by vertebrates and macro-invertebrates may be conspicuous and develop rapidly. In contrast, the effects of plantparasitic nematodes are often more subtle, with gradual declines in plant growth and vigor (Schomaker and Been, 2006). None the less, this group of root herbivores can have strong effects in managed and natural ecosystems as well. For example, the soybean cyst nematode Heterodera glycines Ichinohe (Tylenchida: Heteroderidae) was responsible for >50% of the estimated diseaserelated yield reduction in soybeans grown in the USA from 1996 to 1998 (Wrather et al., 2001), and root-knot nematodes Meloidogyne spp. reduced coffee yields in Hawaii in 1994 by an estimated 20–25% (Koenning et al., 1999). In a South Dakota grassland, nematodes consumed an estimated 6–13% of net annual primary root production (Ingham and Detling, 1984). While nematode feeding tends to reduce host performance, it has been shown that moderate nematode root herbivory can increase plant growth. Bardgett et al. (1999) found that low-density infestations of H. trifolii Goffart (Tylenchida: Heteroderidae) increased white clover growth by 141%. In the same study, they found that H. trifolii grazing on clover also increased the growth of neighboring perennial ryegrass by 217% (Bardgett et al., 1999), potentially due to enhanced nitrogen transfer from wounded clover plants to neighboring grasses (Ayres et al., 2007). It is fairly simple to imagine the impact of an individual root herbivore on a single root. However, scaling up from this simple act of herbivory to an understanding of how root herbivory influences cycling of carbon and nutrients within ecosystems has proven difficult (Brussaard, 1998). A recent study on canopy feeders suggests a strategy that might be adapted for studies of root herbivores. In this case, Frost and Hunter (2004) examined linkages between consumption of leaf tissues by the eastern tent caterpillar, Malacsoma americanum Fabricius (Lepidoptera: Lasiocampidae), and the cycling of carbon and nitrogen via deposition of frass. By collecting frass and redistributing it among a range of potted oak seedlings, they were able to track some of the frass-derived nitrogen as it was taken up by the plants, but they also found a significant quantity leaving the mesocosms in leachate. Similar experiments, either in mesocosm pots or in field-scale plots, might be able to address the potential biogeochemical effects of root herbivory. Although we may have little direct knowledge of their effects on root systems, root herbivores most certainly have a strong effect on nutrient cycling and root dynamics. The emergence of both annual and periodical

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cicadas (Homoptera: Cicadidae) represents a significant translocation of nitrogen aboveground (Callaham et al., 2000). Their synchronized emergence from the soil, followed by large-scale mortality, results in a pulse of nitrogen availability that stimulates the growth and seed production of understorey plants (Yang, 2004, 2006). Similarly to these strong effects on nutrient cycling, herbivores can have strong influences on root demography and production patterns. Applying insecticidal drenches around the root systems of apple trees resulted in a significant increase in root lifespan (Wells et al., 2002). Additions of granular insecticide (chlorpyrifos) to soil cores resulted in a nearly twofold increase in root biomass production after a 9-month period (Stevens and Jones, 2006a). By consuming root tissues and converting them to frass, root herbivores likely contribute significantly to particulate organic matter content of soil, as well as an increase in organic soil carbon concentrations. Given these potentially strong effects on soil resource dynamics, the patchiness of herbivore distributions in space may reinforce soil heterogeneity. Clarifying the range of potential influences of root herbivory requires an explicit consideration of temporal and spatial heterogeneity. Root herbivore densities demonstrate patchiness across multiple scales, a phenomenon common across a range of soil fauna (Ettema and Wardle, 2002). There are a number of techniques that can be used to assess field densities in comparison with economic injury thresholds, including trapping emerging adult insects, collection of soil cores, small-scale excavations or the use of groundpenetrating radar (Johnson et al., 2007). Research designed to address the role of root herbivore density on plant communities, though, requires manipulation of root herbivore density in replicated plots. Some root feeders such as white grubs are easy to collect in large numbers from sod farms (e.g. Stevens et al., 2007b), while others such as M. incognita may be amenable to culture in the lab. Root herbivore amplification is an effective way of addressing this spatial variability, and allows researchers to create densities that reflect a range of levels of management concern. For example, a project might include a treatment with few, if any, herbivores (using either biological or chemical control), one with a low density of herbivores (representing densities below the economic injury threshold), and one with densities simulating outbreak conditions beyond the economic injury threshold. These sorts of experiments are necessary to provide a comprehensive understanding of the influence of root herbivory on biogeochemical cycles in plant communities.

10.5. Root Herbivore Foraging Responses to Soil Heterogeneity Root herbivores are likely to respond to cues produced within the soil that are indicative of resource patches, such as high carbon dioxide (CO2) concentrations (Jones and Coaker, 1977; Brown and Gange, 1990; Johnson and Gregory, 2006). As a result, densities of root herbivores in the field will likely be higher in nutrient-rich patches that are rich in plant roots. It seems likely that roots in nutrient-rich patches, therefore, are more vulnerable to root herbivores. This potential vulnerability is supported by two recent studies of nutrient

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patch–root–herbivore interactions. In the first of these, net root production over a 9-month period was assessed using ingrowth cores in a mixed pine– hardwood forest in South Carolina, USA. Soil was collected from the ingrowth cores in early spring, sieved to remove roots and then returned to the cores; this soil was amended with either fertilizer or granular insecticide, with neither (control) or with both. After 9 months, the soil cores were collected to assess the production of roots over the course of the study. Insecticide additions nearly doubled the root biomass in the cores at harvest; this effect was greater in fertilized than unfertilized patches (Stevens and Jones, 2006a). The same authors conducted a complementary study in the glasshouse, in which they compared the morphological precision and sensitivity to heterogeneity among three common herbaceous species found at the site (Andropogon ternarus Michaux, Eupatorium compositifolium Walter and Solidago altissima L.). When they added root herbivores (white grubs, Coleoptera: Scarabaeidae) to mixed-species experimental pots, the biomass gain of the most precise forager (E. compositifolium) was significantly reduced, while the other, less precise foragers showed no response to the root herbivores (Stevens and Jones, 2006b).

10.5.1. Insect root herbivores These two studies support the concept that the effects of root herbivores vary significantly based on nutrient heterogeneity, and that the effects of root herbivores increase with fine-scale increases in soil fertility. However, neither provided conclusive evidence of root herbivore foraging in nutrient-rich soil patches. At coarse spatial scales, root herbivores appear to find roots by cues such as CO2 emissions from roots and soil organic matter (Johnson and Gregory, 2006). Plant volatiles appear to influence the attractiveness of CO2 signals, making them either more or, in some cases, less attractive (Brown and Gange, 1990; Johnson and Gregory, 2006). There are a number of studies that support the ability and tendency of root herbivores to detect fine-scale variability in soil CO2 concentrations, and to use these differences for orientation during foraging. The threshold level for response to CO2 varies among root herbivore species, from as low as 0.02 mmol mol−1 in the case of the wireworm, Ctenicera destructor Brown (Coleoptera: Elateridae) (Doane et al., 1975). Black vine weevil larvae (Otiorhynchus sulcatus Fabricius) demonstrated a similar sensitivity to CO2, responding to increases in CO2 concentration as small as 0.03 mmol mol−1 (Klingler, 1958). Although behavioural studies conducted on the clover root weevil (Sitona lepidus Gyllenhall) found no attraction to point sources of CO2, the weevils did increase localized searching responses when exposed to CO2 concentrations similar to those emitted from the roots of its host plant (Trifolium repens L.) (Johnson et al., 2006). CO2 increases of 0.125 mmol mol−1 attracted larvae of the western corn root worm, Diabrotica virgifera virgifera LeConte (Coleoptera: Chrysomelidae) (Bernklau and Bjostad, 1998). This response by D. v. virgifera led to attempts to exploit this attraction for the purposes of control; the researchers incorporated artificial sources of CO2 (e.g. yeasts, sucrose

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pellets or even effervescing tablets) into soils in the greenhouse and field to disorient and starve neonates (Bernklau et al., 2004). Adding these ‘artificial’ sources of CO2 led to protection of corn seedlings in some cases. Additional interference with root herbivore foraging can be caused by simultaneous manipulations of fertility and root biomass. A recent study comparing the short-term influence of mineral and organic patches on tree seedling–root herbivore interactions found that white grub larvae were attracted to organic-rich fertilizer patches created using composted cow manure, but not to patches created using slow-release mineral fertilizer (Stevens et al., 2007b). These differences in foraging over the 2-month study period resulted in stronger effects of the grubs on plants in mineral-fertilized pots, where their distribution was more uniform, than in organic pots, where the grubs were more concentrated. In studies of foraging decisions of Sericethis geminata Boisduval (Coleoptera: Scarabaeidae), a root-feeding scarab that can be a pest in pastures in Australia, larvae were more attracted to patches containing live roots than to manure patches. In feeding trials, this species also showed discrimination among patches of varying root density; these grubs appeared to prefer high-density root patches to low-density patches (Wensler, 1971). Despite these fairly clear results in individual trials, combinations of cues complicated the issue: addition of manure reduced the tendency of the grubs to discriminate among patches of varying root density (Wensler, 1971); the authors suggested that this effect may have been the result of the manure obscuring live root cues such as root respiration or the production of root exudates. An intriguing issue arises when one considers these laboratory-foraging studies of white grubs in the context of observations from the field. While white grubs appear to be attracted to nutrient-rich patches, in the field, their densities appear to decline with increasing soil organic matter concentration (Dalthorp et al., 2000; Potter and Held, 2002; Dimock, 2004). The precise mechanism for this decline is unclear. It may be that the natural enemies of soil insects perceive and respond to organic matter cues, in much the same way that they respond to plant secondary compounds produced from roots fed upon by root-feeding insects (Van Tol et al., 2001; Rasmann et al., 2005). The natural enemies of insect root herbivores are also likely to display the aggregated distribution that is common to soil fauna in general (Ettema and Wardle, 2002). The mechanisms that underlie natural enemy heterogeneity, including the contribution of soil heterogeneity, plant root density or the presence of host species, are often unknown for many natural enemies.

10.5.2. Root-feeding nematodes CO2 is thought to be an important cue for long-range host location (measured in centimetres) not only by insect root feeders (see above), but also by plantparasitic nematodes (PPNs) (Robinson, 2002). Once the nematode has located the root zone, however, other substances such as root exudates may assist in the location of individual roots (Perry, 2005). Not all roots are equally

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attractive to a given nematode species, which may contribute to the finescale heterogeneity in nematode distribution. Spiegel et al. (2003) demonstrated that the PPN, Ditylenchus dipsaci Filipjev (Tylenchida: Anguinidae) may move towards or away from root exudates depending on host plant species. PPNs often have preferred sites of penetration along the root (Karssen and Moens, 2006), and may aggregate near certain root regions (Zhao et al., 2000). Such aggregation may be related to fine-scale variation in exudate composition along the root (Perry, 2005). The distribution of roots in the soil may evidence heterogeneity not only in space, but also in time, creating an additional challenge for foraging root feeders. Some root feeders have a resting stage, which allows them to persist through periods of host scarcity to emerge when the probability of host encounter is more favorable. Exposure to host plant exudates has been shown to increase egg hatch in Globodera pallida, G. rostochiensis, M. triticoryzae Guar (Tylenchida: Heteroderidae) and H. glycines Ichinohe (Tylenchida: Heteroderidae) (Schmitt and Riggs, 1991; Gonzalez and Phillips, 1996; Gaur et al., 2000); and the differences in the egg hatch responses of Globodera spp. to host cues may ultimately contribute to observed patterns of relative abundance of each nematode at the field scale (Gonzalez and Phillips, 1996). Although passive dispersal of PPNs in runoff water, wind blown soil or contaminated agricultural equipment may contribute to their distribution at the landscape scale, their active dispersal ability is limited. PPN movement is on the order of 0.15 to 1 m month−1 (reviewed in Robinson, 2002). When reared in the laboratory, a single host plant typically supports numerous nematode generations over weeks or months. This makes autoinfection, where the progeny infects the same host plant initially infested by the parent, likely to be common in the field. In citrus, the burrowing nematode, Radopholus similis (Cobb) Thorne (Tylenchida: Pratylenchidae), migrates from older plant roots to newer growth (Schomaker and Been, 2006). The meagre dispersal ability of nematodes coupled with a propensity for autoinfection may lead to a feedback mechanism that favours localized high-density populations of root-feeding nematodes in the field. Indeed, even in agricultural orchards where the distribution of host plants is quite regular, it is not uncommon for a localized infestation to occur in a few trees that spreads only very slowly to adjacent trees over subsequent years. Thus, plant-parasitic nematodes both respond and contribute to soil heterogeneity at multiple spatio-temporal scales.

10.6. The Multiple Effects of Entomopathogenic Nematodes on Root Herbivores 10.6.1. Introduction to EPNs EPNs are obligate insect parasites, which exhibit a complex life history that is intimately associated with symbiotic bacteria. They have been isolated from every continent except Antarctica; approximately 48 species of EPNs are found in two separate, convergently evolved lineages: the Steinernematidae

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(38 described species) and the Heterorhabditidae (10 species). Only one stage of the life cycle, the infective juvenile (IJ) stage, exists outside the insect host. IJ stage EPNs do not develop, feed or reproduce, existing solely for the purpose of finding a suitable insect host. Once an IJ finds a host, it resumes development and releases its colony of symbiotic bacteria. These bacteria reproduce within the infected host, serving as a food source for the invading nematode(s), and contributing to the mortality of the insect host. EPNs pass through 1–3 generations within the host; ultimately, in response to declining nutritional quality within the host, a new generation of IJs develops and emerges from the cadaver into the soil to find a new host. Individual species of EPNs differ both in their host range as well as the foraging strategies they demonstrate. Their host range includes a variety of rootfeeding insects, including such notable examples as the root-boring ghost moth, H. californicus Boisduval (Lepidoptera: Hepialidae), the Japanese beetle, Popillia japonica Newman (Coleoptera: Scarabaeidae) and the citrus root weevil, D. abbreviatus. Their foraging strategies vary along a continuum from sit-and-wait (ambush) foragers such as S. carpocapsae Weiser (Rhabditida: Steinernematidae) and S. siamkayai Stock, Somsook and Reid (Rhabditida: Steinernematidae) to cruising foragers such as S. glaseri Steiner (Rhabditida: Steinernematidae), with many of the species exhibiting behaviours intermediate between these two extremes (e.g. H. bacteriophora Poinar (Rhabditida: Heterorhabditidae) and S. feltiae Filipjev (Rhabditida: Steinernematidae). These foraging behaviours appear to play some role in the distribution of these species in soils.

10.6.2. EPN heterogeneity and interactions with host insects EPNs are patchily distributed in their natural habitats (Stuart and Gaugler, 1994). While they demonstrate differences among species in the extent of aggregation (Stuart and Gaugler, 1994; Campbell et al., 1996), each of the species demonstrates some degree of aggregation. H. bacteriophora is considered to be one of the most aggregated species, and has been found in densities of 65 IJs cm−2 of soil surface (Lewis et al., 1998). Comparisons of the distributions of H. bacteriophora and S. carpocapsae in a mixed-species community found that the distribution of S. carpocapsae was less patchy than that of H. bacteriophora (Campbell et al., 1996). In this study, though, both of the species were more patchily distributed than their hosts, suggesting other mechanisms (such as soil texture, fertility or alternate or phoretic hosts) must be important components of the spatial patterns we see in field populations. This study also confirmed that within the patches of H. bacteriophora, the populations of their putative host, P. japonica, were decreased relative to patches where the nematodes were absent. Thus, natural EPN populations can reduce their host populations. EPNs that are introduced to various commodities to control insect pests are applied at a homogeneous rate of 2.5 billion IJs ha−1. Despite their initial even distribution at application, within weeks (or even days) this distribution becomes patchy (Wilson et al., 2003), and indeed reflects the distribution

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observed in native populations. This heterogeneity in distribution is constant among EPNs. What drives and reinforces this particular structure of populations remains only partly understood. Aspects of the life history and biology of EPNs contribute to their heterogeneous distribution. Because they are obligate insect parasites they must reflect the aggregations of their hosts, which include root-feeding insects. Within 1–2 weeks’ time an insect host is infected, and as many as 300,000 or more new IJ EPNs emerge from the host cadaver. This mass emergence also contributes to an aggregated distribution, particularly as they move only short distances without the aid of phoretic associations (Eng et al., 2005; Campos-Herrera et al., 2006). Although EPNs have been isolated from habitats across all continents except Antarctica, our knowledge of their biology and ecology in field soil is limited. Typical field manipulations have focused on the influence of a range of factors on their efficacy as biological control agents. The majority of information that is known regarding their natural habitats has been work conducted on the bush lupine–ghost moth–EPN system at Bodega Marine Reserve; even this long-term study site represents only a small portion of the range of bush lupine and ghost moths, and it is unclear whether EPNs exert similarly strong control elsewhere along the California coast. Field research on the effects of introductions for biological control, or on the mechanisms that drive the persistence of local isolates, has generally been limited, but is an increasing focus for current research (Cabanillas et al., 1994; Campbell et al., 1995; Strong et al., 1996; Millar and Barbercheck, 2002; Gruner et al., 2007). The patchy distribution of EPNs in field soils has been attributed to one or more mechanisms that are not mutually exclusive. Dispersal behaviour, host range, the high number of IJs produced from a single infected insect, as well as edaphic factors are each likely to play a role. Recent research points to another interesting factor that may influence distribution: the response of infectivestage EPNs to previously infected insects. Early work by Grewal et al. (1996) demonstrated that insects infected by EPNs were more attractive to EPNs of the same species than uninfected insects. Additional work has shown that EPNs will continue to enter an infected insect host for several days (Campbell and Lewis, 2002; Christen et al., 2007). This attraction to previously infected insects may act to further aggregate EPN populations within field soil.

10.6.3. Responses to soil cues Foraging IJ EPNs are sensitive to a range of chemical cues, some of which are directly associated with the insect host. CO2 seems to play a major role in the foraging behaviour of some EPN species, particularly in the case of cruise-foraging species like S. glaseri. Comparisons between S. glaseri and S. carpocapsae (an ambush forager) showed that S. glaseri responded to hostvolatile treatments that contained CO2, while S. carpocapsae showed little or no response to CO2 or any of the other host-associated cues that were tested (Lewis et al., 1993). Each of the cruise-foraging Steinernema spp. tested has

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demonstrated similar sensitivity to host volatiles (Campbell et al., 2003), suggesting that nutrient-rich soil patches that contain host insects may attract EPNs, even if those insects are not root herbivores. Ambush foraging species, which spend a significant portion of their foraging time nictating (standing on their tails) only respond to volatiles such as CO2 after host contact (Lewis et al., 1995). Some nictating nematodes will also jump at passing insects; host contact is not required in this case (Campbell and Kaya, 2000). Most of the research conducted to date has examined EPN responses to CO2 produced by the host insect, rather than CO2 produced by roots and resource patches in the soil. Infected insects produce CO2, and exhibit distinctive peaks in CO2 production as an infection progresses. However, while there is a pattern of CO2 production by infected insects (Ramos-Rodriguez et al., 2007), there is no evidence that CO2 functions as a long-distance foraging cue for S. carpocapsae, S. glaseri or S. riobravis (Ramos-Rodriguez et al., 2007). Given the many sources of CO2 in the soil (including not only infected and uninfected insects, but also plant roots and organic matter), CO2 may represent a coarse foraging guide for EPNs, suitable for identifying promising foraging locations rather than precisely locating hosts. This is much the same mechanism that has been suggested for root herbivore foraging in response to CO2 (Johnson and Gregory, 2006). The suite of specific compounds that are associated with infected insects and damaged roots may represent a more precise guide for nematodes attempting to find a host insect. These infected insects produce discrete quantities of nitrogen-containing compounds. Approximately 47 mg of nitrogen was lost from greater waxworms, Galleria mellonella L. (Lepidoptera, Pyralidae), after they were infected by EPNs (Shapiro et al., 2000). This nitrogen loss followed a predictable pattern: in the first 3 days after infection, a very small amount (50 µg) of nitrogen was released as volatile ammonia; as the infection progressed, nitrogen leaving the cadavers shifted from inorganic to increasingly organic forms of nitrogen (Shapiro et al., 2000). This suggests that infected insects themselves may represent dynamic resource ‘patches’ for plants, although it is unclear whether such small patches would be of sufficient scale to stimulate root foraging in nearby plant roots. This ammonia release may be a factor that EPNs can use to assess host suitability; small amounts of ammonia (equivalent to production from a newly infected host) attracted foraging nematodes, while higher concentrations were repellent (Shapiro et al., 2000). Given the wide range of concentrations of nitrogen found in the soil, as well as the range of inorganic and organic forms that may be available, the extent to which these laboratory results translate to nematode-foraging behaviour in field settings remains unclear. The attraction of EPNs to plant secondary compounds produced in response to herbivory has been an area of increasing interest. We have known for some time that EPNs are attracted to compounds released from plant roots (e.g. Bird and Bird, 1986; Choo and Kaya, 1991; Van Tol et al., 2001), but we have had little information about the specific compounds that lead to this response. Recently, though, the compound β-caryophyllene has been shown to attract EPNs; in this case, it is β-caryophyllene produced by the roots of

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some varieties of corn (Zea mays L.) when they are fed on by D. v. virgifera (Rasmann et al., 2005). In this study, H. megidis was attracted to small amounts of β-caryophyllene, either when the compound was produced by damaged roots or added artificially to the soil around undamaged plants. This increased nematode presence reduced the impact of D. v. virgifera. This story becomes even more interesting when one considers that the ability to produce β-caryophyllene has been lost or suppressed in many commercial Z. mays strains (Rasmann et al., 2005). Although not all EPN species demonstrate an attraction to β-caryophyllene (K.O. Spence, 2007, unpublished data), these sorts of successes have stimulated further research into the identification and characterization of the broad range of plant volatiles and examination of their potential effects on herbivores and natural enemies, with the ultimate goal of harnessing the production of these volatiles to confer crop protection from shoot and root herbivores (Tholl et al., 2006; Turlings and Ton, 2006).

10.6.4. Indirect effects on plant-parasitic nematodes When EPNs are applied to soil at a rate of 25 cm−2, it is unlikely that their impact will be limited to reducing the density of target pests. Indeed, there is growing interest in the unexpected influences that EPNs might have on soil food webs and nutrient cycling. The first suggestion that unexpected interactions were taking place came from the results of a glasshouse trial showing that repeated applications of S. glaseri resulted in a reduction of M. incognita populations on potted tomatoes (Bird and Bird, 1986). Subsequent to this test, several laboratory, greenhouse and field trials have been conducted to measure the impact of EPNs on PPNs. These tests have been diverse, with different combinations of EPNs and PPNs, different host plants and different measurements of impact. Obviously, synthesizing hypotheses about what is happening is challenging. The initial impetus for this work was the thought that EPNs might offer an alternative to currently used chemical nematicides. However, in most cases, the level of reduction in PPN populations that occurs would not be an acceptable PPN control for growers (Lewis and Grewal, 2005). Not controlling PPNs to the level that satisfies a grower does not mean that there is no interaction. Many of the tests conducted have shown statistically significant reductions in PPN populations after EPN applications. What is surprising is that there is any interaction at all. The two types of nematodes do not compete for any common resources; nor are they direct antagonists to each other. Three hypotheses that are not mutually exclusive have been proposed to explain the interaction: (i) EPN applications could stimulate the growth of general nematode antagonists; (ii) EPNs could behaviourally interfere with PPNs since they are both attracted to roots in the soil; and (iii) EPNs or their bacteria produce materials toxic to PPNs. The symbiotic bacteria of the EPNs produce chemicals that are toxic to many PPN species (Grewal et al., 1999; Boina et al., 2008), and the cell-free extract produced from growing the bacteria in vitro is able to kill M. incognita IJs. This is the current frontrunner of these three hypotheses.

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As we start to understand more about the relationships between EPNs and other soil inhabitants, the underlying drivers of heterogeneity may be better understood. We know that EPN populations are patchy, but we are unsure of why patches are located where they are. In addition, these patchy EPN populations influence other soil fauna either directly or indirectly. New understanding adds more layers of complexity to an already complicated system.

10.7. Conclusions It appears that the effect of resource heterogeneity may be to focus activity in resource-rich patches of soil. Creation of resource patches stimulates root proliferation within the patch. These patches also attract root herbivores, either in response to the roots or to the qualities of the patch itself. While natural enemies such as EPNs must at some point respond to specific cues directly associated with the root herbivores themselves, host finding may be influenced by characteristics of soil fertility (particularly nitrogen compounds), CO2 concentrations or secondary compounds produced by damaged roots. Despite the ability of EPNs to forage through the soil, root herbivores certainly have some refuges from predation. At the Bodega Marine Reserve, for example, significant portions of the site maintain high populations of both the bush lupine and the root-boring ghost moth, but with consistently low or nonexistent populations of EPNs (Gruner et al., 2007). There are a range of potential explanations for the persistence of this enemy-free space. The precise mechanism by which stands of lupine remain nematode-free at Bodega Marine Reserve has yet to be determined; however, root herbivores with an aboveground, strong-flying adult phase will able to disperse for greater distances between generations than can EPNs. This will likely ensure that at least some of the root herbivores will develop in areas with fewer natural enemies. In these areas, root herbivores may be attracted to resourcerich patches, which would then represent areas of increased risk for precise-foraging plants (Stevens and Jones, 2006a). Although this chapter focused on the response of plants, root herbivores and their natural enemies to resource heterogeneity, an area of increasing interest is the potential and tendency for these fauna to reinforce and maintain local heterogeneity. Natural ecosystems such as forests exhibit considerable heterogeneity after disturbance (e.g. Pickett and White, 1985; Clinton and Baker, 2000; Guo et al., 2002); however, preferential plant foraging in nutrient-rich patches acts to homogenize the soil. As a result, heterogeneity may decline rapidly as the system proceeds through the recovery phase (Guo et al., 2002, 2004). By concentrating nutrients in their frass, and leading to resultant stress or even mortality of their host plants, root herbivores may represent a significant counterweight to this homogenization. Infected insects produce significant quantities of nutrients such as nitrogen (>40 mg from a single cadaver; Shapiro et al., 2000), and it seems likely that epizootics would cause similar spatial and temporal pulses in ecosystem biogeochemistry.

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Soil is fundamentally heterogeneous at several scales, including spatial and temporal scales that are relevant to not only root herbivores, but also their host plants and natural enemies. This heterogeneity leads to a complex mix of direct and indirect interactions, all mediated by the soil environment. Root herbivores respond to roots, roots respond to herbivores and natural enemies respond to both roots and herbivores, with the life cycles of the fauna contributing to the aggregation observed in the field. Both root herbivores and EPNs are important concerns in agriculture. Effective biological control of root herbivores is possible, but results can be complicated by the inherent heterogeneity within ecosystems. While heterogeneity of soil at the sort of fine spatial scales we discuss here may be difficult to incorporate into agricultural management, our activities and practices can have significant influences on heterogeneity. The fauna that we are concerned with experience this same heterogeneity. Continuing to examine the behaviours of plants, herbivores and natural enemies within the context of heterogeneity may provide some clues to improve the predictability and effectiveness of biological control techniques targeting root herbivores.

Acknowledgements The ideas presented here were supported by a grant from USDA NRICGP to G.N. Stevens (USDA CSREES #05-35107-16135).

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11

Climate Change Impacts on Root Herbivores

J.T. STALEY1 AND S.N. JOHNSON2 1

Imperial College, Silwood Park, Berkshire, UK; 2Scottish Crop Research Institute, Dundee, UK

11.1. Introduction There is a general consensus among scientists that the earth’s climate is currently changing at a more rapid pace than at any point in its history, due to anthropogenic activity (IPCC, 2007). The average mean surface temperature increased by 0.6°C in the 20th century, the occurrence of unusually warm years has also increased, snow cover has decreased and there have been regional changes in rainfall patterns (Houghton et al., 2001). Since industrialization, the concentrations of gases such as carbon dioxide (CO2) and methane (CH4) in the atmosphere have increased, due to the burning of fossil fuels and changes in land use. For example, the average global atmospheric concentration of CO2 increased by >30% from 280 ppm in 1750 to 360 ppm in 2000 (Houghton et al., 2001), and is predicted to increase further to between 700 and 1000 ppm by the end of the 21st century (Meehl et al., 2007). The build-up of greenhouse gases, such as CO2, traps more solar energy in the lower atmosphere, and is one of the main causes of climate change (Hulme et al., 2002). Global mean temperatures are predicted to rise by about 3°C by the end of the 21st century (Meehl et al., 2007). Within Europe, warming is predicted to be greater during the summer in the Mediterranean region and greater during the winter in parts of northern Europe (Christensen et al., 2007). Annual rainfall is predicted to increase under current climate change models, but there are considerable temporal and spatial variations in precipitation forecasts. Large areas of the globe are expected to have higher winter precipitation and lower summer rainfall (Meehl et al., 2007). Central and southern Europe are likely to receive substantially less summer rainfall, and experience more summer droughts (Christensen et al., 2007), while northern Europe may have increased annual precipitation, mainly in the winter. Soil moisture is predicted to decrease across large areas of the globe, including central and southern Europe and the subtropics, particularly 192

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during the growing season (Meehl et al., 2007). For example, in the south-east UK, average summer soil moisture may be reduced by as much as 20–40%, depending on the CO2 emission scenario (Hulme et al., 2002). Models predicting soil moisture in northern Europe provide less consistent forecasts. The increase in predicted precipitation may result in increased soil moisture. However, other models predict decreased summer soil moisture due to earlier snowmelt and increased evaporation (Christensen et al., 2007). Extreme climatic events can often have greater ecological impacts than changes in average conditions (Stenseth et al., 2002). In addition to changes in the mean temperature and rainfall, the occurrence of extreme climatic events is very likely to increase under climate change (Meehl et al., 2007). For example, very dry summers such as that of 1995 in the south-east UK, when the total summer rainfall fell below 50% of the long-term mean (Morecroft et al., 2002), are expected to occur in 30% of years by the 2050s, and 50% by the 2080s, under a medium CO2 emissions scenario (Hulme et al., 2002). This particular part of Europe is therefore likely to suffer an increased incidence of summer drought. The severity and frequency of predicted summer droughts varies according to the emission scenario used, but even under a low emission scenario there is likely to be some increase in the occurrence and severity of drought during the summer (Hulme et al., 2002). Changes in precipitation patterns due to climate change are predicted to occur across the globe, though the direction and magnitude of the predicted change varies with the season and region (Houghton et al., 2001). Rainfall is predicted to increase at high northern latitudes and in Antarctica, while decreases are likely in most subtropical land regions (IPCC, 2007). Increased variability in annual rainfall is expected in most regions (Meehl et al., 2007). The global climate is therefore predicted to change at a rapid rate, both in terms of average climatic variables such as rainfall and precipitation, and increases in the incidence of extreme events and the variability of the climate. Here, we review the potential direct and indirect (i.e. plant-mediated) impacts of climate change on root-feeding invertebrates and consider how climate change may affect interactions between root- and foliar-feeding herbivores (see Johnson et al., Chapter 9, this volume). While we briefly consider climate changes impacts on root-feeding nematodes, this chapter focuses more on insect herbivores since plant parasitic nematodes have already received attention elsewhere (e.g. Neilson and Boag, 1996).

11.2. Direct Impacts of Climate Change on Root Herbivores Bale et al. (2002) and Hodkinson and Bird (1998) suggest that soil fauna may be buffered from the direct impacts of climate change, and root herbivores are therefore likely to be less responsive to climate change than aboveground phytophages. CO2 concentrations in the soil are generally higher than those in the atmosphere, so soil invertebrates are already adapted to high levels of CO2 (Haimi et al., 2005). In addition, the soil environment may be buffered to changes in temperature, which is less variable in the soil than aboveground, especially

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in the lower soil profiles (Bale et al., 2002). However, small changes in temperature can have a large effect on the rate of invertebrate development, so even relatively minor temperature increases may alter the phenology of some rootfeeding species (e.g. Pearce-Higgins et al., 2005). Reduced soil moisture can have strong impacts on root feeders’ feeding and oviposition behaviour, survival and abundance, particularly in the growing season when most root herbivore feeding and activity peaks occur (Andersen, 1987; Brown and Gange, 1990). It is thus likely that climate change will have direct impacts on root herbivore phenology and abundance, predominantly through reduced soil moisture and temperature changes in the upper soil profile, as discussed below.

11.2.1. Temperature impacts on root herbivore phenology Field experiments have shown that Tipulidae (commonly known as craneflies) are highly responsive to environmental factors (see Blackshaw and Kerry, Chapter 3, this volume). Larvae of several Tipulidae species (leatherjackets) feed on roots in the top few centimetres of the soil profile where temperature varies more than in the lower profiles, and their larval and pupal development is temperature-dependent (Butterfield, 1976). Coulson et al. (1976) conducted reciprocal soil core transfer experiments between sites that differed in temperature along an altitude gradient, in the Pennines in northern England. A reduction in average temperature of 2°C increased pupal duration from 23 to 42 days in the species Molophilus ater Meigen (Diptera: Tipulidae), and from 20 to 22 days in Tipula subnodicornis Zetterstedt (Diptera: Tipulidae) (Coulson et al., 1976). Analysis of temperature and Tipulidae emergence data has shown emergence to be highly correlated with May temperature, as every 1°C increase results in an advance of emergence peak of 7 days, and there is a general trend towards earlier emergence over the last three decades (Pearce-Higgins et al., 2005). Tipulidae emergence is predicted to advance 12 days by the end of the 21st century, which may have implications for breeding birds that rely on them as a food source for feeding chicks (Pearce-Higgins et al., 2005). Increased soil temperatures are also predicted to alter the phenology of cabbage root fly, Delia radicum L. (Diptera: Anthomyiidae) larvae (Collier et al., 1991). Simulation models predict that an increase in average soil temperature of 3°C would result in an earlier and more extended spring emergence of adult D. radicum, and a larger third generation in the late summer. An increase of 5°C would result in a fourth generation across southern UK. However, different biotypes exist with different requirements for diapause, and laboratory studies have shown that populations with no diapause requirement can easily be selected. Collier et al. (1991) therefore suggest that D. radicum may be a species that adapts quickly to climate change, and this potential for adaptation illustrates the difficulty in making accurate predictions of climate change impacts for individual species. None the less, Tipulidae and D. radicum provide examples of root feeders that are likely to be affected by small increases in temperature, and these changes in phenology could have serious repercussions for the ecology of other species in the same food chains, both aboveground and belowground.

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11.2.2. Soil moisture impacts on root herbivore performance and abundance In addition to responding to temperature, several Tipulidae species are also vulnerable to desiccation. Soil water content during egg hatch and the first larval instar may be an important factor in larval survival, and in timing of oviposition for T. paludosa Meigen (Diptera: Tipulidae), while adult survival may be reduced under low air humidity (Coulson, 1962). The development of other root-feeding species may also be delayed in dry soil conditions, as many Coleopteran eggs need to imbibe water prior to hatching (Brown and Gange, 1990), and some Elateridae larvae increase water uptake through the cuticle prior to moulting (Evans and Gough, 1942). Root-feeder abundance may be reduced under conditions of reduced rainfall or low soil moisture. For example, the population density of the root-feeding aphid Pemphigus betae Doane (Hemiptera: Aphididae) is correlated to the previous summer’s rainfall (Moran and Whitham, 1988). Manipulative field experiments provide further evidence for the importance of soil moisture for this species, as abundance, adult size and fecundity of aphids were reduced on plants with limited water supply, compared to well-watered controls (Moran and Whitham, 1988). Mortality of Cyrtomenus bergi Froeschner (Hemiptera: Cydnidae) is increased in the dry season, during which burrowing by the adults to lower soil levels is inhibited by a low soil water content (Riis and Esbjerg, 1998). The abundance of first- and second-instar larvae of the weevil Sitona hispidulus Fabricius (Coleoptera: Curculionidae) was found to be correlated with soil moisture as well as root-nodule availability from an analysis of population structure in lucerne fields, though abundance of older larvae was unaffected by soil moisture (Quinn and Hower, 1986a). Diptera larvae are also dependent on the moisture status of upper soil profiles, as a soil core transfer experiment showed that their populations were reduced at low moisture contents (Briones et al., 1997).

11.2.3. Climate change impacts on nematodes The abundance of micro-invertebrate root feeders is also likely to be altered by climate change. Many nematode species are highly sensitive to soil moisture and temperature. Neilson and Boag (1996) suggest that virus-vector nematodes may become more of a problem for UK agriculture under climate change, as species that currently have distributions that are restricted to the southern UK are likely to expand northwards. Populations of the root-knot nematode Meloidogyne incognita were found to be much higher on white clover (Trifolium repens L.) growing under drought than on plants growing in irrigated plots (McLaughlin and Windham, 1996). The response of herbivorous nematodes in natural habitats to climate change may be harder to predict than that of dominant nematode species in agricultural habitats. Ruess et al. (1999) used cloches to simulate the impact of soil warming on two subarctic habitats in northern Sweden. They found that under increased temperatures there is likely to be a shift in nematode

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community structure towards plant- and fungal-feeding nematodes, but the strength of treatment effects varied both with nematode species and plant community (Ruess et al., 1999). In contrast to the increase in nematodes predicted in response to drought in agricultural habitats, reciprocal core transfer and irrigation experiments in a grassland habitat in North America resulted in a 71% increase in herbivorous nematodes under increased irrigation (Todd et al., 1999). Cyst formation of some root-feeding nematode species may be impeded by drought (e.g. Van der Stoel and Van der Putten, 2006). Nematodes in natural habitats may therefore be more variable in their response to climate change than those in agricultural habitats.

11.2.4. Climate change impacts on root herbivore behaviour Root herbivore behaviour may be altered under climate change, which could affect interactions with their host plants. Several species of herbivorous larvae are known to feed lower down the soil profile in response to drought (Lafrance, 1968; Villani and Wright, 1990). For example, Jones (1979) found that under low soil moisture, feeding damage by carrot fly, Psila rosae Fabricius (Diptera: Psilidae), larvae is confined to below 15 cm soil depth, and few larvae were present. In contrast, under high soil moisture, feeding damage occurred from 1 cm below the soil surface along the whole length of the host plant root. Temperature had less of an impact than soil moisture, as high temperatures only reduced larval feeding damage in the top 2 cm of the soil (Jones, 1979). The oviposition behaviour of soil-dwelling herbivores can also be altered by low soil moisture, which can result in eggs being oviposited at a deeper soil depth (Gray et al., 1992) or fewer eggs being produced (Allsopp et al., 1992). For example, the mole cricket, Scapteriscus borellii Giglio-Tos (Orthoptera: Gryllotalpidae), delays oviposition at low soil moistures, resulting in fewer eggs being laid (Hertl et al., 2001). Reduced soil moisture and increased temperatures have thus been demonstrated to have direct impacts on the development rate, behaviour and abundance of a variety of root-feeding species. While responses to climate change vary depending on the physiology and behaviour of the individual species, the majority of studies on macro-invertebrate root feeders have shown reduced abundance or worse performance, or both, under conditions of low soil moisture. Even slight changes in temperature may result in changes in phenology, which could affect interactions with host plants and other fauna, both aboveground and belowground.

11.2.5. Case study one: summer drought impacts on Elateridae larvae and Coccidae Many Elateridae (Coleoptera) larvae are root feeding (e.g. Agriotes spp.), and several species are important agricultural pests (Parker and Howard, 2001); thus their biology is better understood than that of many root-feeding insects

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in natural systems. In Europe, Elateridae eggs are usually laid in April–June in damp conditions (Miles, 1942), and the depth at which eggs are laid increases if soil moisture levels are low (Furlan, 1996). During the first week after oviposition the eggs absorb water and swell to one and a half times their original size (Furlan, 1996), so moist soil is necessary for egg development and successful hatching. Larval development can take 4–5 years in some Agriotes spp. (Miles, 1942), and includes periods when the larvae do not feed (Evans and Gough, 1942). Peak larval activity and feeding periods occur in the spring and autumn in Europe (Parker and Howard, 2001). Several field and laboratory studies have shown that the depth at which wireworms feed is strongly related to soil moisture. Lafrance (1968) found that soil moisture was the environmental factor that most strongly determined the depth at which five species of wireworm were found in Quebec. During the spring and autumn, wireworms were found in the top 25 cm of soil, while from June to the end of August they were usually deeper in the soil. However, following heavy rain they returned to the topsoil for a few days during the summer (Lafrance, 1968). Seal et al. (1992) also found that in dry, hot weather larvae of two Conoderus spp. move down the soil profile. Agriotes spp. larvae are also found deeper in the soil during the summer, probably in response to both high temperature and low soil moisture near the soil surface (Parker and Howard, 2001). An early laboratory study using Limonius californicus Mannerheim larvae demonstrated that when presented with a moisture gradient, larvae congregated at soil moistures of 8–16% (Campbell, 1937). If they were confined to certain sections of the gradient, over 90% of larvae died at moistures of 24%. Agriotes spp. larvae aggregated in damp (65% water content) sand compared to dry (10%) sand and moved around more under dry conditions, possibly because they were searching for a more favourable environment (Lees, 1943). Agriotes spp. larvae also congregate in soil at 17°C, when offered a choice between this and soil at either 11.5°C or >21°C, and move more quickly at higher temperatures (Falconer, 1945). Soil moisture can affect Elateridae larval development rate indirectly. Temperatures are lower and food supply may be limited in the lower soil profiles where larvae feed during drought periods, and thus development rate is reduced (Furlan, 1998). Although individual wireworms consistently avoid dry soil, relating wireworm population levels to factors such as rainfall or soil type within an agricultural context has so far met with little success (Fryer, 1942; Parker and Seeney, 1997), with the exception of one study in an oak woodland habitat, which showed that Elateridae species abundance was correlated to the number of frost-free days and total annual precipitation (Penev, 1992). It is difficult to separate the impacts of high temperature and soil moisture in observational field studies that relate climate to root phytophage distribution, as the two often co-vary (Villani and Wright, 1990). A manipulative field experiment in which drought and enhanced rainfall treatments had been applied to grassland plots for 10 years provided an opportunity to separate the effects of temperature and precipitation on the abundance of wireworms and other root herbivores (Staley et al., 2007a).

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Soil cores were collected from control (no rainfall manipulation), summer drought (a complete drought during July and August, imposed using rain shelters) and enhanced summer rainfall treatment plots (20% increase in ambient weekly rainfall, see Sternberg et al., 1999 for further details of treatments) in the spring and autumn of 2003 and 2004. However, hot, dry weather conditions during 1 of the 2 sampling years meant that soil moisture in the control and summer drought treatments were very similar, and much lower than soil moisture under the enhanced rainfall treatment. Thus, in dry years the ambient ‘control’ conditions resembled those under the drought treatment, while the enhanced rainfall treatment provided a constant, unstressed comparison to the summer drought from year to year (Staley et al., 2007a). Larvae of the dominant Elateridae species, Agriotes lineatus, were more abundant under the enhanced rainfall treatment, compared to the summer drought treatment and a control treatment that received ambient rainfall (Fig. 11.1A, Staley et al., 2007a). This result confirms the findings of observational field studies and behavioural laboratory studies. In contrast, abundance of root feeder, Lecanopsis formicarum Newstead (Hemiptera: Coccidae), was not altered by the summer rainfall manipulations (Fig. 11.1B, Staley et al., 2007a). Lecanopsis formicarum was also unaffected by dry conditions in laboratory

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experiments, and it has been suggested that it may have evolved in desert and steppe conditions and is thus resistant to desiccation (Boratynski et al., 1982). In contrast, Elateridae larvae may be particularly vulnerable to dehydration as their cuticles are very permeable to water (Evans and Gough, 1942). Although the majority of published studies have shown a reduction in root herbivore numbers under low rainfall, the abundance of root herbivores partly depends on the physiology and evolutionary origin of individual species.

11.3. Plant-mediated Climate Change Impacts on Root Herbivores In this section, we address how aspects of global climate change are likely to affect some of the major aspects of root growth and function, and how these changes may in turn affect root herbivores. It is beyond the scope of this chapter to exhaustively review all of these changes in root growth and function, which are covered in greater detail in the excellent reviews of Rogers et al. (1994) and Van Noordwijk et al. (1998). The effects of climate change on herbivores that feed on aerial parts of the plants have received extensive attention (see review by Bezemer and Jones, 1998). In contrast, the impacts of climate change on root-feeding herbivores are generally poorly understood, despite extensive evidence that climate change will dramatically alter root dynamics and physiology (Norby et al., 2000 and papers therein). The consequences of climate change on roots can be highly specific to plant species, making it difficult to generalize (Van Noordwijk et al., 1998). However, it is possible to make some reasonable assumptions about how climate change, and especially elevated atmospheric CO2, will affect root herbivores on the basis of how roots will be affected by climate change.

11.3.1. Impacts on root growth The impacts of elevated CO2 on roots have been studied for over 150 plant species, with the majority of studies focusing on agronomic crop plants (Rogers et al., 1994). The most commonly measured root response is root dry weight, which for the majority of plants, increases in relative proportion to shoot dry weight under elevated CO2 concentrations (Rogers et al., 1994; Pritchard et al., 1999). Rogers et al. (1994) present a synthesis of the effects of elevated CO2 on four primary root responses (root dry weight, root/total shoot ratio, root length and root number) and concluded that in the majority of plants studied so far, these were positively affected by elevated CO2. In a subsequent review of 264 studies, Rogers et al. (1996) reported that there was increased root growth (relative to shoot growth) under elevated CO2 conditions in 60% of cases, with a mean increase of 11%. In particular, elevated CO2 seems to be associated with increased production of lateral roots rather than elongation of root axes, resulting in highly branched thin roots that are closer to the soil surface (Pritchard and Rogers, 2000). In terms of the likely effects

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that these changes will have on root-feeding herbivores, it could be argued that they will also respond positively to the greater availability of root biomass. For example, Masters et al. (1993) suggest that when nutrients are redirected away from the roots to compensate for foliar herbivory aboveground, this results in a decline in both root biomass and root herbivore performance. It therefore seems reasonable to assume that in some cases the root herbivore performance will be enhanced with greater root availability (Brown and Gange, 1990), although this could be moderated by reduced nutrient availability (see Section 3.2). Since elevated CO2 can cause plants to have highly branched root systems, which are both finer and shallower (Gregory, 2006), these systems are likely to be beneficial for many of the smaller root herbivores, which can only feed on finer roots and have limited burrowing capabilities within the soil profile (Brown and Gange, 1990). The impact of increased temperature on root growth has also received attention (Payne and Gregory, 1988; Gregory, 2006), although in terms of global climate change studies, temperature appears to be generally less influential on root structure and growth than elevated CO2. Most studies have reported either modest increases in relative root growth rates or no effect at all (Rogers et al., 1994). However, when considered in combination with elevated CO2, the effects on root growth can be more pronounced. For example, red maple (Acer rubrum L.) and sugar maple (A. saccharum Marshall) showed increased production and turnover of fine roots in response to higher temperature and CO2 concentrations (Wan et al., 2004), which could also be beneficial for smaller root herbivores in terms of chewing and mobility. Soil water conditions have direct impacts on root herbivores, but they may also indirectly affect root herbivores through changes to root growth. Using over 1300 records of root growth in water-limited environments (≤1000 mm mean annual precipitation), Schenk and Jackson (2002) demonstrated that when canopy size was taken into consideration, the absolute rooting depth increased with increasing levels of precipitation. However, for a given biome, there are many examples of herbaceous plants (except trees and shrubs) producing more extensive root systems in drier soil conditions (Gregory, 2006). In the context of global climate change, where drought conditions are likely to be followed by sudden re-wetting, there are surprisingly few studies on root growth patterns (Gregory, 2006). In one such study with Lolium perenne L., Jupp and Newman (1987) showed that initiation and growth of lateral roots increased by 300–500% as soils became drier, with subsequent elongation of existing laterals following re-wetting. Such sporadic flushes of root growth would probably be tracked by root herbivores, which would themselves migrate up the soil profile and become more active to take advantage of this resource availability (e.g. Jones, 1979). The feeding guild of the root herbivore could be an important determinant of how plant-mediated impacts will affect them. For example, in one of the few studies to address this issue, Salt et al. (1996) investigated the impacts of elevated CO2 on the root biomass of Cardamine pratensis L. and its effect on the abundance of a phloem-feeding root aphid, Pemphigus populitransversus Riley (Homoptera: Aphididae). While they reported that root biomass increased

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under elevated CO2 concentrations, root aphid populations were unaffected, perhaps reflecting that the nutritional quality of phloem sap was not discernibly different even though there was more root tissue available.

11.3.2. Impacts on nutrient uptake In addition to changes in root growth and structure, elevated CO2 has been shown to alter root functions such as water and nutrient uptake, which could have direct effects on the nutritional suitability of roots for belowground herbivores. A range of studies suggest that elevated CO2 can promote water uptake and/or water use efficiency by roots (Davis and Potter, 1983; Garbutt et al., 1990). Moreover, nutrient uptake by roots can also increase under elevated CO2 regimes (Geethakumari and Shivashankar, 1991; Delaire et al., 2005), but the relative concentrations of nutrients in root tissues tends to decline because of increased plant biomass (Yelle et al., 1987; Cotrufo et al., 1998). This is analogous to the situation aboveground, where foliar biomass increases in response to elevated CO2, but the C/N ratio also increases making the foliage less nutritious for folivores (Bezemer and Jones, 1998). Under such circumstances, it is common for foliar herbivores to consume more foliage to compensate for this (e.g. Docherty et al., 1996), so it seems reasonable to expect similar patterns to emerge for belowground herbivores feeding on less nutritious roots. Unlike most folivores, root feeders have the capacity to remove far more plant tissue than they actually consume because large parts of the root system become detached when they sever primary roots (Murray and Clements, 1992, 1998). Any increased rates of feeding by root herbivores could therefore limit extra root growth occurring due to climate change, but to our knowledge this has yet to be determined experimentally. Temperature can also shape nutrient uptake patterns (Clarkson et al., 1988), with several examples of higher temperatures increasing nutrient uptake efficiency (Rufty et al., 1981; Bassirirad et al., 1993). This seems to occur more frequently for nitrogen and phosphorus uptake in plants living in warm and fluctuating habitats rather than colder and stable environments (Bassirirad, 2000). However, even if nutrient uptake efficiency was improved, associated increases in root biomass due to elevated CO2 (see Section 3.1) could actually reduce the relative concentrations of nutrients in root tissues, so root herbivores will most likely experience more root biomass, but of lower nutritional value. Drought is generally assumed to reduce nutrient uptake efficiency for most plants (Gregory, 2006). In Holm oak (Quercus ilex L.), a reduction of 15% in soil water conditions diminished the plant’s uptake of mineral nutrients, with a 40% decrease in root phosphorus concentrations and mobilization of phosphorus to the leaves (Sardans and Penuelas, 2007). It might be expected that root herbivores would be negatively affected by this reduction in nutritional quality, but again this may be dependent on feeding guild of the root herbivore. When plants are stressed aboveground, this frequently leads to

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mobilization of nitrogen compounds in the phloem (usually as amino acids) (Huberty and Denno, 2004), which is often beneficial for sucking herbivores, but detrimental for chewing insects (Koricheva et al., 1998). It is therefore possible that similar patterns occur belowground, for example, if root aphids are benefited from root stress.

11.3.3. Impacts on symbiotic root–microbe associations Roots play a crucial role as sites of symbiotic interactions with soil microbes, including arbuscular mycorrhizal (AM) fungi and N2-fixing Bradyrhizobium bacteria. The impacts of elevated CO2 and temperature on both of these associations are gradually becoming better understood (Soussana and Hartwig, 1996; Fitter et al., 2000, 2004), but the consequences of these climatically induced changes on root feeders remain almost entirely speculative. The case study presented in Section 11.3.4 is perhaps one of the few to experimentally address this issue, and showed that elevated CO2 promoted nodulation in white clover (T. repens L.), which also enhanced the performance of the clover root weevil, S. lepidus Gyllenhall (Coleoptera: Curculionidae). While relatively few studies have reported decreased colonization by AM fungi in response to elevated CO2 and temperature, generalizations remain elusive as both increase and null responses are reported equally frequently (Staddon and Fitter, 1998; Fitter et al., 2000). Soil water conditions are very important for infectivity of AM fungi; for example, periods of drying and wetting have been shown to increase the infectivity of Acaulospora laevis, but decrease the infectivity of Glomus invermaium (Braunberger et al., 1996). The interactions between AM fungi and root herbivores have been studied in a limited number of cases, so the effects of climate on these interactions remain hypothetical. However, even small changes in colonization rates or composition of AM fungi can have important impacts on the performance of root feeders, as illustrated by Gange et al. (1994) for root-feeding vine weevil larvae, Otiorhynchus sulcatus Fabricius (Coleoptera: Curculionidae). In this study, it was demonstrated that larval survival decreased from 84% on AM fungi-free plants to 43% when roots were infected with G. mosseae. Moreover, in addition to being affected by AM fungi some root herbivores can actually affect how well AM fungi colonize roots. Currie et al. (2006), for instance, showed that root herbivory by leatherjackets (T. paludosa) significantly increased colonization by two species of AM fungi (G. mosseae and G. intraradices). Climatically induced changes to root–microbe associations could therefore have a significant impact on both the performance and community dynamics of root herbivores, which in turn could affect the nature of the root–microbe association.

11.3.4. Case study two: elevated CO2 and the clover root weevil Elevated atmospheric CO2 has been reported to promote N2 fixation across a range of legume species and legume-containing systems (Soussana and

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Hartwig, 1996; Zanetti et al., 1996; Hungate et al., 1999) through several mechanisms, including larger numbers of N2-fixing symbiotic bacteria in the rhizosphere (Schortemeyer et al., 1996), more nodules housing the N2-fixing bacteria (Ryle and Powell, 1992), enhanced nitrogenase activity (Norby, 1987) and compositional increases of legumes in the plant community (Newton, 1991; Winkler and Herbst, 2004). Soil-dwelling weevils belonging to the genus Sitona are reported to specifically consume root nodules on several legumes (Byers and Kendall, 1982; Quinn and Hower, 1986b; Wolfson, 1987; Gerard, 2001), so climatically induced changes to nodulation patterns are likely to affect such root feeders. Recent research investigated the impacts of ambient (380 µmol mol−1) and elevated (700 µmol mol−1) CO2 concentrations on the root system of white clover (T. repens L.) and determined how these changes affected the clover root weevil (S. lepidus Gyllenhal) (S.N. Johnson, 2007, unpublished data). A detailed account of the biology of S. lepidus is given in this volume by Goldson and Gerard (Chapter 7). In brief, adult S. lepidus feed on foliage aboveground, where the females lay eggs on or around the base of plants which are eventually carried into the soil surface by rainfall. When the eggs hatch, the emergent larvae burrow into the soil and begin to attack the root system. In particular, the newly hatched larvae frequently attack root nodules that house the N2-fixing Bradyrhizobium bacteria (Hackell and Gerard, 2004; Johnson et al., 2005), which results in enhanced larval performance compared to larvae feeding on roots alone (Gerard, 2001). In this study, T. repens were grown in growth chambers that realistically replicated spatial and temporal air and soil temperature patterns (Gordon et al., 1995). Soil temperature at 10 cm followed a damped lag function of air temperature, whereas soil at 55 and 110 cm remained constant at 12°C. Plants were grown within cages inside the chambers for 7 weeks before introducing individual female S. lepidus weevils to half of the plants at both CO2 concentrations. Insects were allowed to feed on foliage and lay eggs for a further 4 weeks, before harvesting all plants. Most aboveground plant biometrics were unaffected by elevated CO2, with the majority of the effects occurring belowground. In particular, T. repens root mass increased significantly when grown under elevated CO2 (Fig. 11.2A). A striking feature was the increased nodulation that occurred in elevated CO2, with plants grown under these conditions possessing twice as many root nodules as those grown at ambient CO2 (Fig. 11.2B). Similar increases in nodulation and N2 fixation in T. repens have been reported in response to elevated CO2 in both long-term field trials (Newton et al., 1994; Zanetti et al., 1996) and glasshouse experiments (Ryle and Powell, 1992). None of these studies addressed the impacts of these changes on root-feeding insects, but results presented here suggest that the greater number of root nodules was associated with a much larger population of S. lepidus larvae (Fig. 11.2C). More S. lepidus larvae resulted in greater number of damaged nodules (Fig. 11.2D) and indeed there was a strong correlation between nodule number and larval abundance (Fig. 11.2E). This is consistent with the strong positive correlation between the availability of root nodules and larval

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performance reported by Gerard (2001). The increased levels of damage to root nodules caused a dramatic reduction in root nitrogen levels, most probably due to impairment of N2 fixation (Fig. 11.2F). This example illustrates how climate change can modify the dynamics of root-feeding herbivores by affecting root functions such as nodulation and N2 fixation.

11.4. Climate Change Effects on Indirect Interactions Between Root Herbivores and Aboveground Herbivores Root herbivores can affect aboveground invertebrate communities through changes to the chemistry or physiology of a mutual host plant (as discussed by Johnson et al., Chapter 9, this volume). This chapter discusses how studies to date have illustrated that root feeders have greater impact on foliar feeders than vice versa. There is potential for these interactions to be altered under climate change (Schroter et al., 2004), though the scarcity of published studies in this area makes it difficult to draw any general conclusions.

11.4.1. Drought impacts on root herbivore interactions with aboveground herbivores Root feeders may induce a ‘stress response’ in their host plant that leads to an accumulation of free amino acids and carbohydrate in the foliage, which can benefit foliar phytophages on the same plant. Masters et al. (1993) compare this to a plant’s stress response to drought, suggesting that root phytophages remove fine roots, which are important in water uptake. For example, root-chewing insects have been shown to induce water stress in L. perenne L. (Ridsdill-Smith, 1977), and in ash (Fraxinus excelsior L.) artificial root damage and drought had a similar effect on plant physiology, as under both treatments feeding by the ash bud moth, Prays fraxinella Bjerklander (Lepidoptera: Yponomeutidae), increased (Foggo and Speight, 1993). Gange and Brown (1989) demonstrate that the positive effect of root herbivory on the foliar phytophage Aphis fabae Scopoli (Homoptera:Aphididae) can be reduced under a high water treatment, providing further evidence that the mechanism for this interaction is sometimes an induction of host drought stress. There is therefore potential for the strength of these indirect interactions to be increased under climate change, under the additive impacts of summer drought and root herbivores. However, this effect of drought is not consistent across host plant species and experimental systems. Staley et al. (2007b) found that A. lineatus larvae had a negative impact on the performance of a leaf miner, Stephensia brunnichella L. (Lepidoptera: Elachistidae), but that under an extreme drought treatment the leaf miner’s performance was so reduced that the root herbivore had no additional effect on its performance, and the interaction did not occur. The impacts of drought on plantmediated interactions between root herbivores and aboveground species are thus likely to be idiosyncratic, and differ from one host plant to the other.

Climate Change Impacts on Root Herbivores

(B)

3.0 CO2: F1.54 = 36.22 P < 0.001 Insect: F1.54 = 0.01 P = 097

Root mass (g) (mean ± SE)

2.5 2.0 1.5 1.0 0.5

200 180

Number of root nodules (mean ± SE)

(A)

205

160

CO2: F1.54 = 117.97 P < 0.001 Insect: F1.54 = 0.15 P = 0.69

140 120 100 80 60 40 20

0.0

0

(C)

60

CO2: F1.26 = 14.16 P < 0.001

50 Larvae recovered (mean ± SE)

380

700

40 30 20 10

(D) Number of damaged nodules (mean ± SE)

380

80

CO2: F1.26 = 24.50 P < 0.001

60 40 20

80

r = 0.63 P < 0.01

700

380

700

Atmospheric CO2 concentration (µmol mol−1) (F) 50

70 60 50 40 30 20 10

Root nitrogen concnetration (mg g−1 dry mass) mean ± SE)

380

Number of larvae

100

0

0

(E)

700

40

CO2: F1.54 = 3.05 P = 0.087 Insect: F1.54 = 45.68 P = < 0.001

30 20 10 0

0

50

100 150 200 250 300

Number of root nodules

380

700

Atmospheric CO2 concentration (µmol mol−1)

Fig. 11.2. Case study illustrating some of the effects of elevated carbon dioxide (CO2) on the root system of white clover (Trifolium repens) and the consequences for root-feeding larvae of the clover root weevil (Sitona lepidus) (S.N. Johnson, unpublished data). Impacts of elevated CO2 on (A) root mass, (B) number of nodules, (C) S. lepidus larvae recovered, (D) number of damaged nodules, (E) the positive correlation between nodule number and larval abundance and (F) root nitrogen concentrations. Grey bars represent plants with S. lepidus present = 380 µmol mol−1; = 700 µmol mol−1).

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J.T. Staley and S.N. Johnson

11.4.2. CO2 and temperature impacts on aboveground–belowground interactions To our knowledge, there are currently no published studies that have investigated the impacts of increasing CO2 concentrations and higher temperatures on indirect interactions between root herbivores and foliar phytophages. However, using what is known about the general patterns in the impacts of climate change on plant growth and quality, it is possible to speculate on some of the potential impacts. An increase in CO2 concentration is predicted to increase plant biomass and reduce plant tissue quality, through an increase in the C/N ratio and possible increases in the concentrations of some secondary metabolites (Bezemer and Jones, 1998; Veteli et al., 2002; Ainsworth and Long, 2005). For example, the concentration of glucosinolates that were induced by foliar herbivore damage was 28–62% greater in Arabidopsis thaliana (L.) Heynh plants grown under elevated CO2, compared to those grown at ambient CO2 levels (Bidart-Bouzat et al., 2005). In contrast, Rossi et al. (2004) found that there was no effect of elevated CO2 on tannin concentration in Myrtle oak, Q. myrtifolia Willd, foliage in response to leaf-chewing and leaf-mining insects. Increased CO2 concentrations may therefore result in stronger induced responses to herbivory in some plant species, which might strengthen root herbivore impacts on foliar phytophage performance, if the interaction is mediated by an induced defensive response, though the response of induced defences to elevated CO2 may vary with host plant. As previously discussed, plants experiencing elevated CO2 conditions tend to possess foliage of lower nutritional quality (Cotrufo et al., 1998), which results in some foliar feeders consuming more foliage to compensate (e.g. Docherty et al., 1996). Such foliar feeders may therefore be more susceptible to even small increases in defensive compounds through increased intake of foliage. Increases in temperature are expected to result in larger plants that generally contain lower concentrations of some groups of secondary compounds (Bale et al., 2002; Richardson et al., 2002; Veteli et al., 2002), although the impact of temperature on induced responses does not appear to have been investigated. If secondary compounds, in general, are likely to decrease in concentration, this may reduce the occurrence of induced defence-mediated interactions between foliar and root phytophages. However, constitutive and induced defences may not respond in the same way to increases in temperature, and this remains to be tested. Increases in temperature may contribute to the effects of drought, as larger plants might be expected to have a higher demand for water. Higher temperatures may therefore increase the predicted impacts of drought on interactions between root and foliar phytophages. In summary, the effect of warmer temperatures on these indirect interactions is likely to be less than the effect of CO2 and drought, though the impact of temperature on induced defences is unknown. Interactions mediated by changes in foliar quality may be enhanced by both drought and elevated CO2. However, most of these suggested patterns are highly speculative.

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11.5. Conclusions The response of root herbivores to climate change has been less well studied than that of aboveground phytophages. None the less, evidence exists that macro-invertebrate root herbivores are likely to be directly affected by climate change, particularly by reductions in soil moisture during their peak activity periods, and changes in temperature that can affect critical diapause and pupation cues. Climate change may also indirectly alter interactions between root phytophages and their host plants, predators (Pearce-Higgins et al., 2005) and fellow herbivores (Gange and Brown, 1989; Staley et al., 2007b). With the exception of research in the Arctic and sub-Arctic (e.g. Ruess et al., 1999), few manipulative climate change experiments have included root herbivores in their long-term sampling programmes. Chapters in this volume demonstrate the importance of root herbivores, both in applied situations and their often overlooked role in natural systems. Climate change is frequently identified as one of the major risks to both managed and natural habitats, and thus it would appear imperative that both macro- and microinvertebrate root feeders be included in future climate change research programmes.

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Climate Change Impacts on Root Herbivores Wolfson, J.L. (1987) Impact of rhizobium nodules on Sitona hispidulus, the clover root curculio. Entomologia Experimentalis et Applicata 43, 237–243. Yelle, S., Gosselin, A. and Trudel, M.J. (1987) Effect of atmospheric CO2 concentration and root-zone temperature on growth, mineral nutrition, and nitrate reductase activity of greenhouse tomato. Journal of

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Species Index

Acacia spp. 84 Acaulospora laevis 202 Acer Acer spp. 138 A. rubrum 8, 138, 200 A. saccharum 68, 134, 200 A. spicatum 138 Adelges tsugae 136 Adelgidae 136 Agriotes Agriotes. sp. 12, 27, 28, 29, 35, 36, 154, 155, 156, 158, 161, 196, 197, 198 A. lineatus 6, 36, 154, 158, 161, 198 A. obscurus 36 A. sputator 36 Agrostis capillaries 6, 61 Agrotis segetum 36 Alnus spp. 138 Anacardiaceae 138 Anaphes Diana 123 Andropogon ternarus 177 Anthomyiidae 36, 164, 194 Aphididae 12, 195, 200, 204 Aphis Aphis sp. 12 A. fabae 156, 159, 204 A. lineatus 204 Apiaceae 138 Aprostocetus vaquitarum 119 Arabidopsis thaliana 205

Asteraceae 138 Avena sativa 12

Bacillus thuringiensis var. israeliensis 42 Barypeithes pellucidus 137, 138, 139, 140 Beauveria bassiana 104 Betula Betula sp. 86, 138 B. alleghaniensis 137 B. papyrifera 138 Bradyrhizobium spp. 26, 27, 202, 203 Brassica B. napus 26 B. nigra 154, 159, 164 B. oleracea 154 Brentidae 136 Brevicoryne brassicae 12

Caenorhabditis elegans 48 Calomycterus setarius 137 Capsella bursa-pastoris 156 Cardamine pratensis 156, 159, 200 Ceratogramma etiennei 119 Chenopodium album 155, 159 Chromatomyia syngenesiae 155, 158, 159 Chrysodeixis chalcites 154 Chrysomelidae 135, 177 Cicadidae 56, 135, 176 Cinara pseudotsugae 86 215

216

Species Index Cirsium palustre 157 Clinopodium vulgare 155, 156 Coccidae 198 Coffea arabica 84 Conoderus spp. 197 Coronilla varia 10 Corylus spp. 138 Costelytra zealandica 115 Cotesia glomerata 164 Cronartium ribicola 135 Cryphonectria parasitica 135 Ctenicera destructor 177 Cucurbitaceae 138 Curculio caryae 26 Curculionidae 3, 5, 8, 22, 26, 29, 37, 77, 78, 79, 80, 115, 116, 118, 121, 126, 135, 136, 172, 195, 202 Cylas formicarius 136 Cylindrocarpon destructans 103 Cyrtomenus bergi 195

Dactylopiidae 123 Dactylopius opuntiae 123 Daktulosphaira vitifoliae 96 Delia D. antiqua 36 D. radicum 36, 154, 164, 194 Dendroctonus Dendroctonus. sp. 78 D. valens 79 Dermolepida albohirtum 24 Diabrotica Diabrotica spp. 135, 157, 166 D. virgifera virgifera 177 Diaprepes abbreviatus 22, 118, 119, 136, 172, 175, 180 Diceroprocta apache 82 Dirca palustris 138 Ditylenchus dipsaci 179

Elachistidae 204 Elateridae 3, 6, 12, 26, 29, 36, 161, 177, 195, 196, 197, 198, 199 Eulophidae 119 Eupatorium compositifolium 7, 177

Fabaceae 120 Fagaceae 138

Festuca arundinacea 7 Folsomia candida 85 Fragaria Fragaria spp. 138 F. × ananassa 154 Fraxinus excelsior 204 Fusarium spp. 103

Galerucella calmariensis 154, 158 Galleria mellonella 182 Globodera G. pallida 38, 43, 47, 48, 179 G. spp. 37, 179 G. rostochiensis 38, 43, 45, 47, 48, 179 Glomus G. intraradices 202 G. invermaium 202 G. mosseae. 202 Gossypium herbaceum 155, 158, 161, 164 Graphium sp. 79 Graphognathus leucoloma 115 Gryllotalpidae 196

Hayhurstia atriplicis 155, 159 Hemerobiidae 105 Hepialidae 13, 171, 180 Hepialus californicus 13, 157, 171, 180 Heterodera H. avenae 37, 45 H. glycines 175, 179 H. schachtii 37 H. trifolii 61, 175 Heteroderidae 37, 38, 48, 61, 172, 175, 179 Heteronychus arator 115 Heterorhabditidae 171, 180 Heterorhabditis Heterorhabditis sp. 13 H. indica 119 H. marelatus 171 H. medidis 8 H. downsei 8 H. bacteriophora 180 Hordeum vulgare 173 Hormorus undulates 137 Hylastes Hylastes sp. 77, 78 H. assimilis 79 H. pales 78, 79 H. porculus 79

Species Index

217

H. radicis 79 H. salebrosus 78 H. tenuis 78 Hylobius Hylobius sp. 77, 78 H. abietis 80 H. transversovittatus 135, 154, 158 H. warreni 77, 78 Hypera spp. 121

Microctonus M. aethiopoides 116, 120, 121, 122, 123, 124, 125, 126, 127, 128 M. hyperodae 125, 126 Micromus tasmaniae 105 Microsoma exigua 121 Molophilus ater 194 Mymaridae 124 Myzus persicae 12, 156, 157

Inopus rubriceps 115 Ips sp. 78, 79

Neotyphodium N. coenophialum 7 N. lolii 7, 126 Noctuidae 6, 12, 36, 161

Laccaria bicolor 85 Lantana camara 158, 159 Lasiocampidae 175 Lecanopsis formicarum 198 Leguminosae 120 Leptographium sp. 78, 79 Limonius californicus 197 Lipaphis erysimi 12 Liriomyza asclepiadis 156 Lissorhoptrus oryzophilus 155, 159 Listronotus bonariensis 125, 126 Lolium perenne 5, 61, 200, 204 Longidorus sp. 84 Lotus corniculatus 9 Lupinus arboreus 13, 157, 171 Lymantria dispar 86, 136 Lymantriidae 136 Lythrum salicaria 135, 154, 158

Macrosiphon euphorbiae 12 Malacsoma americanum 175 Malus spp. 138 Mamestra brassicae 154 Medicago Medicago spp. 120, 124 M. sativa 3, 4, 8, 120 Megoura viciae 156 Melanotus communis 26 Meloidogynae Meloidogyne sp. 84, 175, M. incognita 48, 172, 176, 183, 195 M. hapla 48 M. triticoryzae 179 Metarhizium anisopliae 104 Metrosideros polymorpha 76

Octolasion trytaeum 12 Ophiostoma sp. 79, 135 Opuntia O. ficus-indica 123 O. spp. 123 O. stricta 123 Oryza sativa 155, 159 Ostrinia nubilalis 157 Ostrya virginiana 137 Otiorhynchus O. sulcatus 8, 28, 29, 37, 136, 154, 177, 202 O. ovatus 137

Pachylobius picivorus 78, 79 Pachyrhinus elegans 137 Pemiphigus P. betae 155, 159, 195 P. bursarius 36 Phaeoacremonium spp. 103 Phaseolus vulgaris 25 Phyllobius P. oblongus 137, 138, 139 P. horticola 5, 154, 155, 156, 157, 159 Phyllophaga spp. 23 Phylloxeridae 96 Phytophthora Phytophthora spp. 118, 175 P. ramorum 135 Pieridae 12, 164 Pieris P. brassicae 154, 159, 164 P. rapae 12, 154

218

Species Index Pinus Pinus spp. 136 P. elliottii 80 P. palustris 72, 80, 134 P. resinosa 78, 135 P. strobus 80 P. sylvestris 85 P. taeda 78, 84 P. virginiana 8 Plantago lanceolata 154, 156 Polydrusus sericeus 137, 138, 139 Polyphylla decemlineata 174 Popillia japonica 7, 26, 118, 136, 180 Populus Populus spp. 138 P. deltoides 76 P. tremuloides 138 Pratylenchidae 85, 179 Pratylenchus Pratylenchus sp. 84 P. vulnus 85 Prays fraxinella 204 Pseudomonas spp. 6 Pseudotsuga menziesii 76, 86 Psila rosae 36, 196 Psilidae 36, 196 Pueraria spp. 135 Pyralidae 182 Pyrus spp. 138

Quadrastichus haitiensis 119 Quercus Quercus spp. 138 Q. ilex 201 Q. myrtifolia 205 Q. rubra 138

Radopholus similis 179 Rhabditidae 48 Rhizobium sp. 84 Rhizophora mangle 80 Rhizotrogus majalis 26 Rosaceae 138 Rubus spp. 137

Saccharum officinarum 24 Salix spp. 138 Scapteriscus borellii 196

Scarabaeidae 5, 7, 24, 26, 56, 115, 118, 136, 174, 177, 178, 180 Sciaphilis asperatus 137, 138, 139 Scoliidae 117 Scolytidae 78, 79 Scolytinae 77 Sericethis geminata 178 Sinapis arvensis 12, 155, 156 Sirex noctilio 136 Siricidae 136 Sirococcus clavigigenti-juglandacaerum 135 Sitona Sitona sp. 120 S. discoideus 116, 120, 121, 123, 124, 125, 126, 127, 128 S. hispidulus 3, 4, 8, 9, 10, 11, 136, 193 S. humeralis 121 S. lepidus 4, 5, 9, 26, 27, 116, 120, 121, 122, 123, 124, 127, 128, 129, 177, 202, 203, 205 Solanum Solanum sp. 48 S. sisymbriifolium 48 Solidago altissima 177 Sonchus S. arvensis 158 S. asper 155, 158 S. oleraceus 154, 155, 156, 157, 158, 159 S. palustris 155, 158 Sphaeroma terebrans 80 Sphaeromatidae 80 Spodoptera S. exigua 6, 155, 158, 161 S. frugiperda 155, 159 S. litoralis 12 Steinernema Steinernema spp. 181 S. carpocapsae 180, 181, 182 S. diaprepesi 172 S. feltiae 180 S. glaseri 180, 181, 182, 183 S. riobrave 119 S. siamkayai 180 Steinernematidae 172, 179, 180 Stephensia brunnichella 155, 156, 158, 204 Sternorrhynchae 96 Stratiomyidae 115 Strophosoma melanogrammum 137

Species Index Tachinidae 117, 121, Tamarix Tamarix spp. 135 T. ramosissima 82 Taraxacum officinale 7 Teleonemia scrupulosa 158, 159 Terellia ruficauda 157 Tetraopes tetraophthalmus 156 Tilia Americana 137 Tiphia vernalis 118 Tiphiidae 117, 118 Tipula Tipula spp. 36, 55, 61, 136 T. oleracea 38 T. paludosa 5, 6, 10, 15, 38, 39, 40, 41, 49, 195, 202 T. subnodicornis 194 Tipulidae 5, 38, 55, 56, 137, 194, 195 Trachyphloeus T. bifoveolatus 138 T. aristatus 137, 138 Trichogrammatidae 119 Trifolium Trifolium spp. 120 T. fragiferum 5 T. pratense 3, 9 T. repens 3, 5, 61, 177, 195, 202, 203, 205

219 T. subterraneum 5 Tripleurospermum perforatum 157 Triticum aestivum 12, 26

Ulmaceae 138 Ulmus spp. 138

Verticillium dahliae 46 Vicia V. grandiflora 10 V. sativa 5 Vitaceae 138 Vitis Vitis spp 96, 97, 98, 99, 100, 102, 103, 138 V. vinifera 97, 98, 99, 100, 101, 102, 105, 108, 109

Xyleborus sp. 77

Yponomeutidae 204

Zea mays 157, 183

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Subject Index

Aboveground-belowground herbivore interactions 153–170 effects of elevated carbon dioxide 206 effects of elevated temperature 206 in forest ecosystems 86 Abscisic acid 161 Accelerometer 21, 22, 24 Acoustic detection 16–17, 22–25 background of the technique 22 potential applications 22–23 and root herbivore behaviour 23–25 Aestivation 121, 122, 124, 127, 128 Allelochemicals 161, 163 see also Defence compounds and Secondary compounds Ambush foraging nematodes 180, 181, 182, 189 Ammonium fertilizer 173 soil solutions 10 uptake 86 Ammonia release 182 Antifeedant 126 Attraction of root herbivores to carbon dioxide 177 to nutrient patches 8, 174, 178, 184 phylloxera 100 Autoinfection 179

b-caryophyllene 182–183 Biocontrol see Biological control Biogeochemical cycle 175, 176 Biological control 115–133 citrus fruit weevil 118–119 classical 116 clover root weevil 120–129 colonisation and dispersal 127–128 modelling 128–129 parasitoid selection 121–123 success 121–123 synchrony with host 126–127 inundation 119 management potential 116–118 phylloxera 104–105 potato cyst nematode 47 Biological invasions 135, 143 Biopesticides against leatherjackets 42, 49 Biotypes biocontrol agents 116, 123, 125–126, 128 cabbage root fly 194 phylloxera 99 Body size and plant productivity 57–58 Bottom-up regulation 7, 61 Brown roots 15, 71 Burrowing behaviour 26–27, 37, 195, 200, 203 221

222

Subject Index Cannibalism in leatherjackets 39 Carbohydrates exudation 11, 61 in fine roots 69 mediating abovegroundbelowground interactions 160, 163, 204 Carbon exudation 6, 68 flux in forest ecosystems 71, 73, 74–75, 86, 135, 142 uptake 5 Carbon dioxide host location cue 176–178, 179, 181, 182, 184 climate change impacts 86–87, 192, 193, 205 aboveground-belowground interactions 206 nutrient uptake 201 roots and root herbivores 199–201 Cellulose 69, 74, 87 Chewing behaviour acoustic detection 23 feeding guild responses 161, 162, 166, 200, 202, 206 Chlorophyll 109 Chlorosis 45, 78, 84 Chlorpyrifos 15, 126, 176 Cicadas 68, 81–83 Cicadian rhythm 126 Collembola insecticides 17 mycorrhizal interactions 85 root defences 75 secondary attack 37 Community-Level Physiological Profiles (CLPP) 6, 11, 61 Compact Airborne Spectrographic Imager (CASI) 108–109 Compensation-overcompensatory responses 57–58 Competition plant 7, 15, 16, 62, 135, 174 plant competition mediated by root herbivores 135, 143 potato cyst nematode 44 Cone containers 3 Containers for studying root herbivores 11–14

Cortex 43, 44, 102 Crop rotation 36, 41, 42, 47–48, 49 tolerance 45, 46 Cruising foraging nematodes 180 Cues, location 176, 177, 178, 179, 181, 184 Climate change and root herbivores 192–213 aboveground-belowground interactions 204–206 clover root weevil 202–204 direct impacts 193–199 behaviour 196 nematodes 195–196 performance and abundance 195 phenology 194 Elateridae and coccidia 196–199 forest root herbivores 86–87 plant-mediated impacts 199–202 nutrient uptake 201–202 root growth 199–201 root-microbe interactions 202

Decomposer interactions with root herbivores 12–13, 55, 57, 77 Decomposition of root herbivores 6, 82, 172 Defence induction hypothesis 161 Defence compounds mediating abovegroundbelowground interactions 161, 162–164 forest ecosystems 75–76, 87 see also Allelochemicals and Secondary compounds Denodulation 11, 124 Desiccation OF root herbivores 40, 116, 120, 121, 195, 199 Detrital foodwebs 62 Diapause 120, 122, 128, 137, 194, 207 Dieback 171, 174 Dispersal of root herbivores 36, 80 DNA markers 99–100 probes 102, 109 Drought aboveground-belowground interactions 204

Subject Index

223 biocontrol agents 124 climate change 192–193 Elateridae larvae 196–199 forest ecosystems 77 nematodes 195–196 nutrient uptake 201–202 phylloxera 99 root growth 200 root herbivore behaviour 196

Earthworms in forest ecosystems 143–144 in root herbivore studies 12, 13, 14 Economic thresholds 41, 47 Economic costs of root herbivory in grasslands 58–60 Egg parasitoids 119, 120 123–125, 127 Eggs climate change impacts 195, 196, 197 clover root weevil, 121, 122, 203 leatherjackets 38–40 phylloxera 96, 100, 103 potato cyst nematode 43, 44, 45, 46, 47 rearing in culture 3–4 El Niño South Oscillation cycle 77, 171 Endoparasitoid 121 Endophytes 7, 48, 126 Enemy free space 171, 184 Entomopathogenic nematodes (EPN) 13, 142, 80, 165, 179–184 citrus root weevil 118–119 heterogeneity in soil 180–181 phylloxera 104 plant-parasitic nematode interactions 183–184 response to soil cues 181–183 Entomopathogens 118 Ethylene 161 Exotic invasions 82, 104, 115–116, 119, 123, 125, 135–136, 143–144 Extreme climatic events 193

Feeding preference tests 9 Feeding sites 9, 44, 96, 97, 100, 103, 120, 121 Fenitrothion 126

Fertilizer 8, 42, 45, 59, 73, 172, 173, 177, 178 Field techniques for studying root herbivores destructive 11–14 non-destructive 14–16 Fine roots biomass 68–70 climate change impacts 200, 204 forest ecosystems 70–76, 82–87, 134–135, 137, 142, 143–144 Flooding 174 Food webs 14, 61, 62, 68, 86, 126, 153, 165, 171, 173, 183 Foraging behaviour by entomopathogenic nematodes 179–184 by plants 7, 70,171–174 by root herbivores 8, 37, 174–179 Formononetin 9 Frass 142, 172, 175, 176, 184 Fungi endophytes 7, 126 mycorrizal see Mycorrhizae nematode interactions 44, 84, 119, 126, 196 pathogens 46, 77, 78, 79, 97, 98, 102, 118, 135 phylloxera interactions 103 Fungicide 72

Galls on leaves 96, 97, 99, 103 on roots 83, 96, 100, 102, 103, 105, 107, 120, 154 Gallicicole 99 Gaussian mixtures 25 Geophone 21, 22 Glucosinolates 161, 163, 206 Glycoalkaloids 29 Grow bags 8 Growth chambers 5, 203 Grape phylloxera 96–114 biological control 104–105 chemical control 105 chemical fingerprinting 108 cultural management 104 detection and surveillance 107 eradication 98 feeding physiology 102–103

224

Subject Index Grape phylloxera (continued ) fungal interactions 103 genetic diversity 99–100 history and distribution 97–98 molecular fingerprinting 109–110 population monitoring 101–102 quarantine measures 105–107 resistant rootstocks 98–99 soil environment 100–101 spectral fingerprinting 108–109

Haemocoel 122 Hardwood forests 74, 134, 136, 137, 138, 140, 142, 143, 177 Hemicellulose 69, 74 Heterogeneity entomopathogenic nematodes 180–181 nutrients 7, 172–173 soil 8, 176–179 High Performance Liquid Chromatography (HPLC) 108 Honeydew 118, 124 Host plant ranges 37, 43, 123, 137–138 Hybrid rootstock 97, 98, 99, 101 Hydrolysis 160

Imaging hyperspectral 109 remote sensing 109, 110 X-ray 25–30 Induced defences 161, 162, 163, 166, 206 see also Defence compounds Infective juveniles (IJs) 43, 44, 46, 47, 48, 180, 181, 183 Ingrowth cores 72, 177 Invasive root feeding insects agriculture 118–119 forests 137–149 grasslands 120–129 Insecticide 4, 13, 15, 16, 41, 42, 43, 49, 72, 73, 105, 116, 176, 177 Integrated Pest Management (IPM) 104 Inundative biocontrol 49, 119 Irrigation experiments 16, 105, 196

Jasmonic acid 161, 163

Leatherjackets 38–43 biology and ecology 38–41, 55 climate change impacts 194, 202 crop damage 41 management 41–43 Legumes 3, 9, 11, 27, 61, 84, 202, 203 Lignin 60, 69, 71, 74, 87

Mechanical root damage 165 Meta-analysis 39, 40 Methane 192 Methyl jasmonate (MeJA) 76 Microbial communities 6, 10, 11, 61, 142 control 118 Microcosms 4, 10–11 Micro-elements 163 Micro-lysimeters 4–5 Mineralization 57, 59, 61, 69 Mini-rhizotrons 4, 10–11, 15, 71, 72, 101 Mobility of root herbivores 104, 200 Models 17, 27, 42, 74, 128 Mycorrhizae 68, 69, 70, 83, 84, 85 arbuscular mycorrhizal (AM) 85, 86, 153, 173 ectomycorrhizal (EM) 85

Natural enemies of root herbivores 5, 38, 39, 44, 49, 104, 115, 116, 119–120, 126, 165–166, 171, 172, 173, 175, 178, 183 Nectar 118, 124, 125, 164 Nematicides 47, 48, 183 Neonicotinoid 105 Net Primary Production (NPP) in forests 68, 87, 134 in grasslands 54, 55, 57 Nicotine 161 Nitrogen deposition 63, 81 fertilization 15 fixation 13, 84, 120, 124, 153, 204 plant uptake and tissue content 10, 60, 69, 70, 73–75, 82, 85, 135, 144, 163, 176, 201, 202, 205 root herbivore influenced transfer between plants 10, 61, 175 uptake by herbivores 45, 58, 160, 162, 182

Subject Index Nitrogenase activity 203 Nodosities 97, 102, 103 Nodulation 84, 124, 129, 202, 203, 204 see also Root nodules Non-target effects 105, 116, 119, 125–126 Nuclear Magnetic Resonance (NMR) imaging 108 Nutrient stress hypothesis 162

Oils, weevil tissue 9 Organic C input 10, 100, 176 farming 41, 42 fertilizer 8, 178 N input 182 Outbreaks cicadas 56, 81–83 Ips beetles 79 phylloxera 98, 100, 106 Oviposition and preoviposition 6, 36, 49, 81, 118, 120, 121, 122, 124, 126, 127, 128, 137, 194, 195, 196, 197

Parasitoids aboveground 13, 119–129, 164–165 belowground 39, 44, 118–119 Pericycle 43 Pesticides 14, 41–42, 47, 49, 72, 105, 116, 117, 118, 126 Phenolic and polyphenolic compounds 75, 76, 87, 161 Phloem feeding herbivores 103, 160, 161, 162, 166, 200 transport in plants 69, 70, 162, 202 Phoretic associations 180, 181 Phospholipid Fatty Acid (PLFA) analysis 142 biomarkers 11 Phosphorus 58, 69, 70, 163, 173, 201 Photosynthesis 45, 68, 71, 74, 85, 109, 120, 163, 173 Phylloxera Infested Zones (PIZs) 98, 106, 107 Piezoelectric probe or sensor 21, 22 Plant-stress hypothesis 160 Plant succession 16, 56, 77, 78, 79, 83 Plastic tunnels 8 Pollinator 13, 164

225 Population abundance affected by root herbivores 156–159, 162, 163 crashes of leatherjackets 40 dynamics of root herbivores 42, 50, 100, 101, 102, 128, 140 Potassium 163, 173 Potato cyst nematodes (PCN) 43–48 biology and ecology 43–44 crop damage 44–46 management 46–48 Pupae 9, 38, 118, 122, 127, 137, 194, 207 Pyrrolepyrazine 126

Radiation dose 21, 25, 26, 29 ultraviolet 116, 119 Rainfall and root herbivores 39–40, 171, 195, 196–199 Relative Growth Rate (RGR) 57, 154–159 Resource availability 76, 200 Rhizotrons 14, see also mini-rhizotrons Root architecture 11, 45, 69–70 biomass 6, 8, 15, 16, 55, 57, 68, 69, 73, 83, 101, 144, 163, 176, 177, 178, 200, 201 boring 77–81 defences 75–76, 87 exudation and exudates 6, 55, 56, 57, 59, 61–62, 100, 173, 178–179 foraging 173–174 function 160, 201, 204 knot nematodes 38, 48, 84–85, 175, 195 lifespan 74, 176 proliferation and growth 11, 45, 59, 86, 162, 173–174, 184, 199, 201 shoot ratio 5, 13, 86, 87 volatiles 100, 164–165 r-strategists 120

Salicylic acid 161, 163 Saprophytic fungi 85 Sap-sucking see Phloem feeding Secondary compounds 61, 105, 178, 182, 184, 206 see also Defence Compounds

226

Subject Index Senescence 46, 71–72, 107, 162 Slant boards 3, 4, 8–10, 27 Soil cores 71, 72, 140, 176, 177, 194, 195, 198 food webs 165, 171, 173, 183 heterogeneity 8, 172–173, 175, 176–178 olfactometer 5 pH 44, 100, 103 temperature 106, 140, 194, 203 texture 100, 172, 180 type 73, 83, 101, 121, 124, 197 water 40, 195, 200, 201, 202 Source-sink relationships 163 Spatial aggregation 14 Starch 69, 86, 87 Stress response hypothesis 160–161, 204 Stridulation 24 Sucrose 103, 177 Sugarcane 24, 136 Sugars 6, 11, 29, 69, 70

Tannins 74, 75, 76, 206 Terpenes 43, 76 Top-down regulation 59, 60, 61, 171 Transparent plant pouches 10–11 Trap crops 47, 48 Tritrophic interactions 110, 126, 165 Tuberosities 97, 102

Tuber consumtion by wireworms 27–29, 37

Vector quantization 25 Vertical transmission 118

White roots 70–71 Wireworms aboveground-belowground interactions 161, 164 agricultural pests 35, 36, 37, 49 climate change 196–198 experimental systems 3, 6,12 grassland pests 55 response to carbon dioxide 177 X-ray studies 26, 27–29 Wounds caused by root herbivores 118, 143, 175

Xylem feeder herbivores 81 transport in plants 69, 70, 81 X-ray attenuation 21, 25, 28 beam 21, 26 microtomography 21, 26, 27 radiography 21, 26 scanner 25 tomography 16, 20, 23, 25–30