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Aphids as Crop Pests, 2nd Edition

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Aphids are among the major global pest groups, causing serious economic damage to many food and commodity crops in most parts of the world. This revision and update of the well-received first edition published ten years ago reflects the expansion of research in genomics, endosymbionts and semiochemicals, as well as the shift from control of aphids with insecticides to a more integrated approach imposed by increasing resistance in the aphids and government restrictions on pesticides. The book remains a comprehensive and up-to-date reference work on the biology of aphids, the various methods of controlling them and the progress of integrated pest management as illustrated by ten case histories.

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1: Taxonomic Issues

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1

Taxonomic Issues

Roger L. Blackman1* and the late Victor F. Eastop

1

Department of Life Sciences, The Natural History Museum, London, UK

Introduction

There are more than 5000 species of Aphididae in  the world (Remaudière and Remaudière, 1997;

Favret, 2014). Of these, about 450 species have been recorded from crop plants (Blackman and Eastop,

2000), but only about 100 have exploited the agricultural environment successfully to the extent that they are of significant economic importance (Table 1.1).

The agriculturally important species are mostly in the subfamily Aphidinae, not only because this is the largest subfamily but also because it contains a very high proportion of the aphids that feed on herbaceous plants (Blackman and Eastop, 2006). Some quite large aphid subfamilies – the Calaphidinae and Lachninae, for example – are associated almost exclusively with woody plants, as are most of the smaller ones.

The Aphididae is one of three families of Aphidoidea, the other two being the Adelgidae, or conifer woolly aphids, and the Phylloxeridae, which are also nearly all associated with trees but include the notorious

 

2: Aphid Genomics and its Contribution to Understanding Aphids as Crop Pests

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2

Aphid Genomics and its Contribution to Understanding Aphids as Crop

Pests

Linda M. Field,1* Chris Bass,2 T.G. Emyr Davies,1 Martin

S. Williamson1 and Jing-Jiang Zhou1

1

Department of Biological Chemistry and Crop Protection, Rothamsted

Research, Harpenden, UK; 2Department of Biological Chemistry and Crop

­Protection, College of Life and Environmental Sciences, University of Exeter,

Penryn, UK

Introduction

The International Aphid Genomics Consortium

(IAGC) was ‘born’ at an inaugural meeting in Paris in June 2003, called to coordinate advances in developing aphids as a model system for evolutionary genetics and genomics, to cut down on unnecessary redundancy and to enhance the likelihood of securing funds for a large-scale project. The ultimate goal of this network was to develop the aphid model system to the same level of molecular, cell and developmental biological understanding as other model insects. To this end, it was decided to start by securing funds to sequence the Acyrtho­siphon pisum (pea aphid) genome and the Steering Committee submitted a proposal that was funded by the National

 

3: Population Genetic Issues: New Insights Using Conventional Molecular Markers and Genomics Tools

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3

Population Genetic Issues:

New Insights Using Conventional

Molecular Markers and Genomics

Tools

Hugh D. Loxdale,1* Owain Edwards,2 Denis Tagu3 and Christoph Vorburger4

1

School of Biosciences, Cardiff University, Cardiff, UK; 2CSIRO Land and

Water Flagship, Centre for Environment and Life Sciences, Floreat, Western

Australia; 3INRA, Le Rheu, France; 4Institut für Integrative Biologie ETHZ and

EAWAG, Dübendorf, Switzerland

Introduction

Aphids as pests of crops and their adaptations

Aphids are highly variable morphologically, genetically and behaviourally. It is this large pool of variation that has allowed them to be such globally successful pests of agriculture, horticulture and forestry, not only by damaging plant vigour by tapping into their phloem sap, often as large colonies, but also by transmission of plant pathogenic viruses. This can have huge consequences for the economics of healthy plant maintenance and production consequent upon attack by aphids.

 

4: Life Cycles and Polyphenism

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4

Life Cycles and Polyphenism1

Jim Hardie*

Royal Entomological Society, St Albans, UK, and Imperial College London,

Department of Life Sciences, Ascot, UK

Introduction

Aphids display a diverse range of relatively complicated life cycles associated with seasonal changes and the ephemeral availability of suitable hostplant material. The life cycle is divided into stages characterized by one or more specialist phenotypes/ morphs. Each of these morphs has a specific function that is necessary for the completion of that stage of the life cycle. Typical aphid life cycles have morphs that specialize in sexual and/or parthenogenetic reproduction, population dispersal/migration and surviving less favourable climatic or nutritional conditions. Not all morphs of pest species infest crop plants. How these life cycles, and related morphs, influence the likelihood of aphids becoming crop pests, when at least one host plant has economic significance, and the importance of the different life cycles for applied entomology are reported here.

 

5: Growth and Development

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5

Growth and Development

Simon R. Leather,1* Caroline S. Awmack2 and Michael

P.D. Garratt3

1

Department of Crop and Environment Science, Harper Adams University, Newport,

UK; 2Sexton Close, Daventry, UK; 3Centre for Agri-­Environment Research, School of Agriculture, Policy and Development, University of Reading, Reading, UK

Introduction

The growth and developmental rates of individual aphids have been studied extensively since the early investigations of Davis (1915) because they can be reliable indicators of future population growth rates (Leather and Dixon, 1984; Acreman and Dixon,

1989). In this chapter, we discuss the methods used to measure aphid growth and development, the relationships between these measures of aphid performance, and the reliability of using the results of such experiments to predict the performance of field populations of pest aphids.

Individual aphids frequently have extremely high growth and developmental rates, allowing populations rapidly to reach levels that are damaging to crop plants. Under optimal growth conditions, an individual aphid typically commences reproduction

 

6: Nutrition and Symbiosis

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6

Nutrition and Symbiosis

Angela E. Douglas1* and Helmut F. van Emden2

1

Department of Entomology, Cornell University, Ithaca, USA; 2School of

­Agriculture, Policy and Development, The University of Reading, Reading, UK

Introduction

A single question dominates the study of aphid nutrition: how does plant phloem sap, a nutritionally unbalanced diet of high C:N content, support the remarkably high growth and reproductive rates characteristic of many aphid species? The ‘short answer’ to this question has two elements. First, phloem sap offers a near-continuous supply of small organic compounds, principally sugars and amino acids, which require the minimum of digestive processing; consequently, the assimilation efficiency of aphids is exceptionally high. Second, the key nutritional inadequacy of phloem sap, the low essential amino acid content, is met by symbiotic bacteria in the aphid.

The ‘long answer’ to this opening question requires a mechanistic understanding of aphid nutrition and its interaction with the functions of the symbiotic microorganisms, and this is the topic of this chapter. Research on aphid nutrition has been dominated by carbon and nitrogen nutrition, and these topics are addressed in the third and fourth sections, respectively. The fifth section summarizes our current understanding of the mineral and micronutrient requirements of aphids. First, however, the key features of microbial symbiosis in aphids are reviewed.

 

7: Aphids and Stress

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7

Aphids and Stress

Jeremy Pritchard1* and Laura H. Vickers2

1

School of Biosciences, University of Birmingham, Edgbaston, UK; 2Crop and

Environment Sciences, Harper Adams University, Newport, UK

Introduction

Aphids are a hugely successful insect group, feeding on a broad range of plant species over a wide range of climates. Many host-plant species are important crops, and the impact of aphids on crops through re­source removal, facilitation of pathogens (Chapter 11, this volume) and virus transmission (Chapter 15, this volume) in temperate climates is predicted to increase as climate change alters the environment in their favour (Harrington et al., 1995, 2001, 2004). Aphids feed from the phloem sap of plants; locating and exploiting this non-ideal food source requires a suite of adaptations (Chapter 9, this volume), including symbiosis with bacteria, the significance of which is only just becoming fully appreciated (Chapter 6, this volume). Their specialist feeding within a single cell type gives aphids a particularly intimate association with their host plant. This association makes it is impossible to consider the effects of abiotic stress on aphids in the absence of the plant. We argue that the two most important stressors on aphids and plants are temperature and drought, the latter

 

8: Chemical Ecology

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8

Chemical Ecology

John A. Pickett,1* Toby J.A. Bruce1 and Robert T.

Glinwood2

1

Biological Chemistry and Crop Protection, Rothamsted Research, Harpenden, UK;

Department of Crop Production Ecology, Swedish University of Agricultural

Sciences, Uppsala, Sweden

2

Introduction

The ecology of aphids is, like that of most insects, highly dependent upon signals. Signals from host and non-host plants convey information that is vital for selecting feeding, larviposition and mating sites. Signals from aphids themselves are important in attracting a mate, aggregating with conspecifics, avoiding competition and sensing or giving warning of threats. Chemical signals (semiochemicals) are relatively efficient to biosynthesize, specific, easy to disperse into the environment and, not least, easy to detect. Aphid life cycles are characterized by complex interactions, and those species that alternate between hosts and have a sexual phase are faced with considerable challenges, such as locating the correct winter (primary) host, finding mates, leaving the winter host in the spring and successfully colonizing the summer (secondary) host. Therefore, it is no surprise that aphids make extensive use of semiochemicals, both in gathering information from their environment and in signalling to each other.

 

9: Host-plant Selection and Feeding

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9

Host-plant Selection and Feeding

Jan Pettersson,1* W. Fred Tjallingii2 and Jim Hardie3

1

Department of Ecology, The Swedish University of Agricultural Sciences,

Uppsala, Sweden; 2EPG Systems, Wageningen, The Netherlands; 3Royal

Entomological Society, St Albans, UK, and Imperial College London,

Department of Life Sciences, Ascot, UK

Introduction

Prominent traits in aphid ecology are rapid reproduction and advanced adaptation to host-plant ecology and physiology. This includes host-plant and feeding-site discrimination using sensitive chemosensory information that has proved to be an important research topic over the past few decades

(Chapter 8, this volume). Cues shown to be important in host-plant selection, phloem finding, phloem acceptance and the sensory aspects are described in the sequence of choices from a distance, to the plant surface, to the internal plant factors, and ultimately to phloem feeding.

Visual cues constitute an initial step in host selection for alate aphids and have an important role for approaching and landing on a plant. Different aspects of spectral patterns have been studied with regard to orientation (Döring and Chittka, 2007).

 

10: Aphid Movement: Process and Consequences

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10

�Aphid Movement: Process and Consequences

Alberto Fereres,1* Michael E. Irwin2 and Gail E.

Kampmeier3

1

Spanish Research Council, ICA-CSIC, Madrid, Spain; 2Department of ­Natural

Resources and Environmental Sciences, University of Illinois, Urbana, USA;

3

Illinois Natural History Survey, Prairie Research Institute, University of Illinois,

Champaign, USA

Introduction

This chapter reviews the movement of agriculturally important aphids. It includes information on how different morphs and life stages redistribute themselves in response to intrinsic factors and extrinsic perturbations over time and through

­spatial scales that span walking behaviour on individual plants to aerial transport over very long distances. The chapter explores the economic consequences of aphid movement and weaves the multiple roles of movement into the tapestry of pest management, providing insight into ways of manipulating aphid movement and thereby mitigating the negative economic impacts resulting from it.

 

11: Predators, Parasitoids and Pathogens

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11

�Predators, Parasitoids and Pathogens1

Jacques Brodeur,1* Ann E. Hajek,2 George E. Heimpel,3

John J. Sloggett,4 Manfred Mackauer,5 Judith K. Pell6 and the late Wolfgang Völkl7

1

Institut de Recherche en Biologie Végétale, Département de Sciences B

­ iologiques,

Université de Montréal, Montréal, Canada; 2Department of ­Entomology, ­Cornell

University, Ithaca, USA; 3Department of Entomology, ­University of ­Minnesota,

­St-Paul, USA; 4Maastricht Science Programme, ­Maastricht University, ­Maastricht,

The Netherlands; 5Department of ­Biological Sciences, Simon Fraser University,

Burnaby, Canada; 6J.K. Pell Consulting, Luton, UK; 7Department of Animal Ecology,

University of Bayreuth, Bayreuth, Germany

Introduction

Aphids occur in most terrestrial habitats. They are commonly attacked by predators, parasitoids and pathogens; often collectively termed Aphidophaga

(Völkl et al., 2007). Predators kill their prey by feeding on them. In some families of aphid predators

 

12: Population Dynamics: Cycles and Patterns

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12

�Population Dynamics: Cycles and Patterns

Samuel G. Leigh and Helmut F. van Emden*

School of Agriculture, Policy and Development, The University of Reading,

Reading, UK

Introduction

The aim of the study of population dynamics is to identify the causes of numerical change in a population and explain how the interaction between these causes results in the observed changes.

Figure 13.1, this volume, illustrates many of the components involved. These components have been allocated separate chapters in this volume, and the next chapter takes one important crop pest species, Sitobion avenae (English grain aphid), and uses a modelling approach to illustrate how the components integrate to describe its population dynamics over different spatial scales.

This chapter looks at the abundance on crops of several aphid species and what explanations for the patterns observed can be proposed from fieldderived evidence.

Analyses based on age-specific life tables and key-factor analysis, which are well-established techniques for many other insects (Southwood,

 

13: Aphid Population Dynamics: From Fields to Landscapes

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13

Aphid Population Dynamics:

From Fields to Landscapes

James R. Bell,1* Jean-Sébastien Pierre2 and Charles-Antoine Dedryver3

1

Rothamsted Insect Survey, Rothamsted Research, Harpenden, UK;

UMR 6553, Ecosystèmes-Biodiversité-Evolution, Rennes, France;

3

Institut de Génétique, Environnement et Protection des Plantes INRA,

Le Rheu, France

2

Introduction

There are close to 5000 aphid species in the world, of which about 200 are crop pests. For these pests, never before have decision support systems been in so much demand (Chapter 17, this volume) both to help reduce pesticide use and also to prevent damaging outbreaks. However, for only a handful of these species is there a sufficient level of ecological and biological understanding to merit undertaking a population dynamics approach. Unsurprisingly, the emphasis has been on aphids that cause the most serious crop damage (Table 13.1), and these are firmly our focus. The majority of aphid pest population studies are concentrated within agriculture, particularly on a small number of aphids that use cereals as their host. Rice, wheat and maize provide 60% of the world’s food energy intake, so it is perhaps not surprising that aphids feature heavily as biological threats, particularly in rice and wheat (FAO, 2016). There are considerable amounts of data concerning the ecology of these aphids, and consequently there have been repeated modelling attempts, statistical or otherwise, that have sought to capture and predict their population dynamics. These cereal aphid studies form the backbone of this chapter and will be discussed at length, but we shall also occasionally discuss the dynamics of aphids that use other annual crops and trees as their host.

 

14: Feeding Injury

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14

Feeding Injury

Fiona L. Goggin,1* Sharron S. Quisenberry2 and Xinzhi Ni3

1

Department of Entomology, University of Arkansas, Fayetteville, USA;

­Emeritus, Department of Entomology, Iowa State University, Ames, USA;

3

USDA-ARS Crop Genetics and Breeding Research Unit, Coastal Plain

Experiment Station, University of Georgia, Tifton, USA

2

Introduction

The sternorrychan superfamily Aphidoidea includes aphids (Aphididae), adelgids (Adelgidae) and phylloxera (Phylloxeridae), and all three of these families pose a serious problem in the production of food and fibre crops. In fact, all of the world’s major crops are attacked by at least one species of Aphidoidea, although some plants suffer greater injury than others (Blackman and Eastop, 1994, 2006). The importance of crop losses caused by aphids and other insect herbivores has been described in these terms:

‘The shift of energy from plants to insects rivals in scale mankind’s own demands on the photosynthesizing world’ (Southwood, 1997). Moreover, aphids and other sap-sucking arthropods can extract more energy per unit area than grazers and browsers, and they do so without consuming any of the plant structural tissues (Dixon, 1985). Several well-known introduced pests illustrate the ability of the Aphidoidea to limit crop yields and to have profound ecological and sociological impacts. The Russian wheat aphid

 

15: Transmission of Plant Viruses

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15

Transmission of Plant Viruses1

Mark Stevens1* and Christophe Lacomme2

1

British Beet Research Organisation, Norwich, UK; 2Virology and Zoology

Branch, Science and Advice for Scottish Agriculture (SASA), Edinburgh, UK

Introduction

As obligate parasites, plant viruses need to move from infected to healthy plants in order to survive.

This is achieved either by mechanical means or, in the case of most plant viruses, by exploiting biological vectors such as arthropods, nematodes and fungi.

Of the 700 or more plant viruses (van Regenmortel et al., 2000), about 70% are known, or suspected, to be transmitted by arthropod, nematode, or fungal vectors (Nault, 1997). Sap-feeding insects in the

Auchenorrhyncha and Sternorryhncha are particularly important vectors, transmitting more than

380 viruses (Nault, 1997). The aphids (Aphididae) are by far the most important family among these vectors, transmitting many more viruses than whiteflies (Aleyrodidae), leafhoppers (Cicadellidae) or planthoppers (Delphacidae) (Fig. 15.1). More than

 

16: Monitoring and Forecasting

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16

Monitoring and Forecasting1

Richard Harrington1* and Maurice Hullé2

1

2

AgroEcology Department, Rothamsted Research, Harpenden, UK;

INRA, UMR1349 IGEPP, Le Rheu, France

Introduction

This chapter covers the monitoring and forecasting of aphids: why, what, where, when and how?

Attention to the first four questions is a prerequisite for proper consideration of the fifth.

Why Monitor and Forecast?

Within the context of aphids as crop pests, monitoring and forecasting are aimed ultimately at optimizing the nature, location and timing of control measures, although background research will be necessary ahead of that directly supporting the decision making of individual growers. For example, samples from traps involving attraction to colour could not be translated into sound advice without knowledge of how different species vary in their response to colour. Optimization of control measures involves economic and environmental considerations to varying degrees, depending on the nature of the problem and of the individual trying to solve it. For example, prophylactic use of chemicals may be more desirable for the control of aphids causing virus spread in seed potato crops, where there may be very low tolerance levels for the virus, and hence for the vectors, than for control of aphids causing direct feeding damage in a ware potato crop, where tolerance levels will be higher. A prophylactic approach may suit a wealthy, risk-averse grower with little concern for the environment or longer-term problems such as the build-up of insecticide resistance, whereas advice to reduce inputs may be adopted more readily by those at the other end of the wealth and environmental concern spectra. The degree

 

17: Decision Support Systems

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17

Decision Support Systems

Frédéric Fabre1* and Charles-Antoine Dedryver2

1

INRA, UMR SAVE 1065 F-33882, Villenave d’Ornon, France;

INRA, UMR 1349 Institut de Génétique, Environnement et Protection des plantes, F-35653 Le Rheu, France

2

Introduction

Decision support systems (DSSs) can be defined as user-friendly systems which, through some combination of expert knowledge, simulation models and databases, provide support to decision makers

(Knight, 1997). In plant protection, DSSs typically estimate the need for and the timing of one or several protection measures along the cropping season: they support tactical decisions with short-range objectives (‘one season in a field’), most often when responsive (rather than preventive) tactics are available (Pedigo et al., 1986). DSSs bridge the gap between scientific knowledge and users making day-to-day management decisions. They help farmers to make the right decision, by interpreting complex biological information within an economical context, and by proposing simple choices.

 

18: Chemical Control

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18

Chemical Control

Alan M. Dewar1 and Ian Denholm2*

1

Dewar Crop Protection Ltd, Bury St Edmunds, UK; 2University of

­Hertfordshire, Hatfield, UK

Introduction

As serious crop pests, aphids are major targets for insecticides and help drive a continuing quest for new compounds with novel modes of action and favourable environmental profiles. The first edition of this chapter (Dewar, 2007) noted a progressive change from a market dominated by organophosphates (OPs) and carbamates (Schepers, 1989; Jeschke et al., 2002) towards increasing reliance on pyrethroids and, latterly, neonicotinoids. Over the past

10  years, these changes have continued apace. In many countries, most OPs and carbamates have become obsolete or are being phased out as a consequence of their toxicological profile. Neonicotinoids, as a result of their exceptional efficacy and versatility, have continued to increase in popularity and have been joined by a suite of new molecules with distinct properties and/or modes of action. The carbamoyltriazole, triazamate, an excellent aphicide due to its systemicity and downward translocation in plants (Dewar et al., 1994), had a brief period of use prior to its withdrawal due to environmental concerns.

 

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