Biological Control of Plant-parasitic Nematodes: Soil Ecosystem Management in Sustainable Agriculture

By Graham R. Stirling

Plant-parasitic nematodes are one of multiple causes of soil-related sub-optimal crop performance. This book integrates soil health and sustainable agriculture with nematode ecology and suppressive services provided by the soil food web to provide holistic solutions. Biological control is an important component of all nematode management programmes, and with a particular focus on integrated soil biology management, this book describes tools available to farmers to enhance the activity of natural enemies, and utilize soil biological processes to reduce losses from nematodes.

• Language: English
• Publisher: CAB International
• Release date: May 14, 2014
• ISBN: 9781789243802

Graham R. Stirling

Dr Stirling has 35 years experience in research, has published more than 70 scientific papers and has been made an Honorary Member and Fellow of the Australasian Plant Pathology Society for his services to the Society and to Nematology. He has extensive experience in both temperate and tropical agriculture, having worked in Queensland, South Australia and California on many crops, including wheat, rice, stonefruit, apples, citrus, grapes, pineapples, ginger, sugarcane, tomatoes, potatoes, and other vegetables. Dr. Stirling is recognised internationally for his work on nematodes, particularly biological control, and is also an experienced plant pathologist and soil biologist.

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Foreword

Graham Stirling’s previous book on biological control of plant-parasitic nematodes reflected the state of the science at that time. In the intervening 20 years, our perception of processes regarding the regulation and suppression of nematodes in agricultural ecosystems has become much more holistic. It has been enhanced by advances in our knowledge of the role of soil biota in ecosystem processes, and by research on cropping systems that has been conducted under the auspices of agricultural sustainability initiatives. The current book recognizes that soil organisms function in an intricately connected and interacting food web; that they compete for, or exploit each other as, food resources; and that their activity and diversity is strongly influenced by the ways in which crops and soil are managed.

One might expect a dichotomy of interests regarding approaches to biological control of soil organisms. On the one hand, there is the commercial interest in the identification of specific parasites or predators that have potential for production in mass culture and application to field sites. On the other hand, there is the growing understanding that a plethora of well-adapted organisms occurs in the soil and that, through appropriate soil stewardship, an environment can be developed in which pest species are suppressed by their endemic natural enemies. The two interests seem at odds in that stewardship promoting the development of a suite of naturally occurring antagonists may limit the commercial value of introduced organisms by reducing the required frequency or biomass of applications. This book provides important information that allows a rational synthesis of both perspectives.

Inundative releases of organisms into a diverse and complex system, which has all microsites occupied and exploited, are usually only effective in the short term. The introduced organisms are unlikely to become established unless they possess invasive characteristics that render them more successful than the incumbents. Such an approach is more likely to be successful in systems that have been biologically damaged by previous management, or by lack of resources. For example, inundative releases may be very useful for regulating pest species during the multi-year transition period from a conducive to a suppressive soil environment. Also, in cases where there is no incentive for long-term stewardship of leased or rented land, or in situations where a rapid solution to a pest problem is necessary, inundative releases will be appropriate.

The organisms of the soil differ in physiology and behaviour, and contribute to ecosystem services in a multitude of ways. They occupy, and are variously adapted to, the array of soil micro-niches that is created by distribution of resources, the irregularities of the physical and chemical components of the soil matrix, and gradients of water, temperature and gaseous diffusion. Consequently, the communities of organisms inhabiting each micro-site may differ in physiological and behavioural characteristics. The integral effect of the dynamic interactions at each micro-site represents the magnitude of the service performed by the resident taxa. General and specific suppressiveness to plant-parasitic nematodes is one of the services provided by the soil biota, and examples of situations where it has been enhanced through management are well documented in extremely readable passages in this book.

Over the years between Dr Stirling’s two books, his perceptions of how soil biological systems function have evolved based on his observation and vast practical experience. This book is centred on stewardship of the intrinsic suppressiveness of soils that results from their physical, chemical and biological complexity. Dr Stirling explains that plant residues, root exudates and other organic inputs fuel the biological components of the system, and that the organic resources that would normally drive undisturbed systems have become severely depleted by modern agricultural practices.

Dr Stirling emphasizes that certain agricultural activities, including applications of chemicals, excessive tillage and prolonged fallow periods between crops, are major deterrents to intrinsic biological suppression or regulation of pest species. Soil tillage disrupts soil microhabitats and has abrasive effects on larger-bodied organisms. Most soil organisms inhabit the thin films of water that surround soil particles. Agricultural chemicals applied to the soil dissolve in the water films and their concentrations change with fluxes in water volume. Soil organisms differ in their tolerance to these chemical stresses, but some will be adversely affected. For example, large-bodied nematodes of the nematode orders Dorylaimida and Mononchida include important generalist and specialist predators of other soil nematodes. They are frequently abundant under undisturbed conditions but often they are not detectable in conventionally managed agricultural soils. The effects of agricultural practices are recorded, perhaps indelibly, in the biological, chemical and physical state of the soil; the effects are not easily reversed.

Once a soil has been converted to intensive agricultural production and has lost its natural suppressiveness, pest species become more abundant. One convenient and effective solution is to apply a pesticide. However, many of the pesticides used to control nematodes, and those that have been used in the past, are broad-spectrum biocides that further reduce levels of organisms which might otherwise contribute to natural soil suppressiveness. Thus, stepping onto the pesticide treadmill as a management response to plant damage by plant-parasitic nematodes and other soil pests has long-term consequences: natural suppressive mechanisms are depleted to such an extent that it becomes difficult to discontinue chemical-intensive management. It may be achieved by activating the soil biological community through inputs of organic matter, and eliminating constraining factors (e.g. preventing soil compaction, minimizing tillage, reducing the length of fallows, limiting chemical inputs) but, as Dr Stirling explains, adopting these practices does not result in instantaneous success. Organisms that are missing from the system or are below detectable levels may take many years to return and re-establish. There is a management learning curve during the transition to biologically intensive systems, and the risk of pest-induced losses is greater during the transition. Organic inputs to increase soil carbon and fuel the soil food web will not have the instantaneous effect of a biocide. It may take years of input and continuous stewardship before resource levels are sufficient and the necessary successional changes have occurred in soil communities. Dr Stirling provides examples of systems in which the transition has been successfully accomplished.

A factor often not considered in cropping system design studies is that modern high-yielding crop cultivars that have been selected for high-input agriculture may lack the root mass and morphology for exploitation of organic nutrient sources. These cultivars, when grown under the conditions for which they are selected, do not need an active soil biota. So, perhaps there is a need to select cultivars with different morphological characteristics for biointensive systems. Root exudation and rhizodeposition are major drivers of the soil food web. A larger root system may enhance the priming of biological activity in the soil food web.

This book is about stewardship of the soil ecosystem through management strategies that are continued across years. Here factors and decisions associated with land tenure become important. Management-intensive stewardship is more likely to be applied to land that is owned than to land that is rented and in which there may not be long-term interest, a metaphorical tragedy of the commons. At a global level, agriculture is a net nutrient-export enterprise; there is an urgent need to consider the global cycling of carbon, nitrogen and other nutrients. These minerals are harvested from the soil via the crops that are produced, transported to centres of human population, and then excreted into rivers and oceans. How can the nutrients be returned to the land so that they are cycled rather than permanently exported? How can organic wastes that accumulate around cities and livestock enterprises be used to enhance suppressive services of the soil food web that have been diminished by the constant removal of harvested product?

In the final chapters of this book, Dr Stirling provides a valuable ‘how to’ synthesis for the transition to, and stewardship of, biologically suppressive soils with the goal of minimizing damage due to nematode pests. Hopefully the approaches he has suggested will encourage scientists and land managers to tackle a primary cause of nematode problems in agriculture: practices, or lack thereof, that result in diminution of the soil biota.

Howard Ferris

Department of Entomology and Nematology

University of California, Davis

Preface

My first book on biological control of plant-parasitic nematodes was published in 1991, at a time when biological control was first being seriously considered as an option for managing nematode pests. Several widely used nematicides had been removed from the market in the previous 15 years, and nematologists were seeking alternatives that had little or no impact on human health or the environment. Although research on natural enemies of nematodes was in its infancy, the number of scientists working on biological control was increasing, and their research programmes were being supported by a surge of activity in related areas such as soil biology and ecology.

In the last 22 years, the level of interest in biological control of nematodes has continued to increase, and an ever-expanding group of researchers has addressed numerous issues of relevance to that topic. Some of the key areas of investigation include: the ecology of nematophagous fungi; molecular taxonomy of parasites and predators; regulatory forces within soil food webs and their effects on the nematode community; interactions between bacteria in the genus Pasteuria and various plant-parasitic nematodes; host specificity of Pasteuria spp.; the impact of endophytes, mycorrhizal fungi and plant growth-promoting rhizobacteria on nematodes; nematode-suppressive soils; induced systemic resistance to soilborne pathogens; the role of organic matter in stimulating natural enemies of nematodes; molecular ecology of soil and rhizosphere organisms; and biotic contributions to soil health and sustainable agriculture. Given the amount of new knowledge that has been generated during that period, it is clearly time to review progress and update Stirling (1991).

In considering whether I should attempt to write another book, my initial thoughts were that the field of biological control of nematodes was now so large that it would be impossible for one person to do justice to the topic. However, if biological control is to ever become a key component of future nematode management programmes, there is a need to integrate the large body of existing knowledge into a package that is useful to a diverse audience: fellow scientists who may focus on only one or two biological control agents; students wishing to undertake studies in this fascinating but challenging field; nematologists working in areas other than biological control; plant pathologists, agronomists, horticulturalists, soil scientists, extension personnel, pest management consultants, and others who constantly face soil-related problems but are not conversant with nematode management; and farmers seeking sustainable methods of reducing losses from nematode pests.

Given the breadth of my experience, I decided that I had as much chance as anyone of tackling this task. I was raised on a farm, my family is still farming, and my first degree was in agricultural science; so I have an abiding interest in ensuring that our farming systems continue to become more productive and sustainable. My career commenced in the temperate region of southern Australia, working mainly on grapevines and citrus, but a mid-career move to Queensland enabled me to broaden my experience and work with a number of tropical and subtropical crops, including rice, pineapple, sugarcane and ginger, and a range of vegetable crops. I have also been involved in research for the Australian grains industry, which continues to flourish in some of the poorest soils and most demanding climates in the world. Thus, I have been fortunate to have worked on a wide range of nematode problems in diverse environments. Project and consultancy work in Asia and the Pacific has also given me some awareness of the problems faced by agricultural professionals and farmers in developing countries. Although I have never specialized entirely on biological control, I have worked with egg-parasitic fungi, nematode-trapping fungi and Pasteuria; collaborated with companies interested in developing commercially acceptable biological products for nematode control; and contributed to our understanding of nematode-suppressive soils. Thus, I have broad interests in biological control and believe that it has the potential to play an important role in nematode management.

For 13 years, I was a member of a research group working on yield decline of sugarcane, and my interaction with members of that team (agronomists, soil scientists, soil microbiologists, plant pathologists, agricultural engineers, extension specialists and economists) taught me that problems often considered to be caused by nematodes and soilborne pathogens are actually the result of inappropriate farming systems. Thus, the solution is often to modify the way a crop is grown rather than focus on controlling selected root pathogens. Biological suppressiveness to nematodes can be enhanced by modifying the farming system: a lesson I have learnt through first-hand experience.

Unusually for a research scientist, I have spent about one-third of my career operating a small science-based company that undertakes research and provides diagnostic services in nematodes and soilborne diseases. I am, therefore, aware of the multi-faceted nature of running a business and the need for financial viability. Thus, I have some empathy for land managers, who must face economic realities when dealing with soilborne disease problems. My main clients are grower/government-funded research corporations wishing to see practical outcomes from their research investments, and this explains why a recurring theme in this book is that agricultural research must be relevant to the farming community; that outcomes must be communicated to those who can benefit from the work; and that research is not complete until outcomes are tested, adapted and validated in the field.

One thing I have learnt during my career is that plant-parasitic nematodes are rarely the only cause of suboptimal crop performance. If a poor-growth problem is soil-related, it will generally have multiple causes, and so it is important to provide holistic solutions rather than a temporary fix that just focuses on the nematode component. Biological control has been a continuing interest, but from my perspective, it is only one of many tools that can be used by farmers to improve soil health and limit losses from plant-parasitic nematodes.

Someone with my background will obviously have a different view of biological control than the specialists in many different fields whose contributions are essential for the development and implementation of biological methods of managing nematodes. This book deliberately takes a broad view of the topic and attempts to integrate our knowledge of soil health and sustainable agriculture with our understanding of nematode ecology and the suppressive services that are provided by the soil food web. Hopefully, the end result will be useful to anyone with an interest in agriculture, soil biology or ecology. Since biological control should be a component of all integrated nematode management programmes, the book focuses on the tools available to farmers (e.g. organic matter management strategies, rotation schemes, tillage practices, and water and nutrient inputs) and considers how they might be used to enhance the activity of natural enemies and reduce losses from nematode pests. The mass production and release of biological control agents is also covered, but is not seen as the universal panacea that it is often considered to be.

I do not claim that this book provides a detailed coverage of every subject that is discussed. A voluminous amount of literature is available on ecological and agricultural issues that are pertinent to biological control (e.g. conservation agriculture, sustainable farming systems, soil organic matter, precision agriculture, the rhizosphere, soil health, the soil biological community and regulatory mechanisms within the soil food web) and if additional information on topics of this nature is required, it should be obtained from the cited references. In the same way, review articles and chapters in multi-authored books must be consulted for detailed information on specific aspects of biological control, as they have been written by experts in the particular subject area. However, many such reviews have a relatively narrow focus, whereas this book intentionally takes a broader view and considers biological control of nematodes from an ecological and farming systems perspective. Hopefully it will motivate readers to start thinking holistically about how the nematode community and a diverse range of natural enemies can be manipulated to achieve effective and sustainable systems of suppressing nematode pests.

Although my original intention was to revise my 1991 book, it soon became apparent that a complete rewrite was required. The previous book summarizes much of the early work on biological control of nematodes and remains relevant, but this book is deliberately different. It has a wider focus; the content has been substantially rearranged; and it concentrates on research that has been carried out over the last 25 years. The book has been subdivided into six sections, and after an initial introductory chapter, the second section covers the soil environment and the organisms that live in soil, and how they are influenced by plants and farming systems. The third and fourth sections deal with the natural enemies of nematodes (parasitic and predatory fungi, invertebrate predators, bacterial parasites and viruses), and a diverse range of fungal and bacterial symbionts that have the capacity to interfere in some way with nematode development. Methods of reducing populations of plant-parasitic nematodes through biological means are discussed in the fifth section, with a particular focus on a concept referred to as ‘integrated soil biology management’. The final section summarizes the main points made in the book, and offers some suggestions on priorities for future research. It also includes a chapter that encourages advisors and practitioners to think about the biological status of their soils, and provides guidelines on how soil biological processes can be utilized to reduce losses from nematode pests.

Graham Stirling

August 2013

Acknowledgements

Many people helped me complete this book, but Howard Ferris, Rob McSorley, Andreas Westphal, Sara Sánchez-Moreno, Kathy Ophel-Keller and Mike Bell deserve a special mention. They acted as referees and made many incisive comments on my first draft. Although I take total responsibility for the final version, their contributions are very much appreciated.

My association with Howard Ferris (University of California, Davis) began at UC Riverside in 1975, when I took a one-semester student project and worked with a nematode–grapevine model he had developed. At the time, Howard was compiling the results of a survey which showed that root-knot nematode populations in California peach orchards were unexpectedly low (Ferris et al., 1976). I decided that it would be interesting to find out why, and my PhD studies with Ron Mankau led to the discovery of Dactylella oviparasitica (now Brachyphoris oviparasitica) and its role in suppressing the nematode. Since then, Howard’s wide-ranging contributions in the field of nematode ecology made him an obvious choice to not only comment on an early draft of the book, but also write the Foreword.

I first came across Rob McSorley (University of Florida) when we competed against each other in a student’s presentation session at a meeting of the Society of Nematologists. Rob won the prize, but we remained friends! He spent a sabbatical year with me in Brisbane during the 1980s, and is widely known for his work on nematode ecology and management. Andreas Westphal (Institute for Plant Protection in Field Crops and Grassland, Germany) was another whose comments I sought, as he has worked in many quite different environments in the United States and Europe, and has also made a major contribution to our understanding of nematode-suppressive soils. I have never met Sara Sánchez-Moreno (National Institute for Agricultural and Food Research and Technology, Spain), but her ecological papers are substantive and she has experience with the agriculture in California and southern Europe.

My two Australian colleagues are not nematologists, and so they were able to view what I had written from a different perspective. Kathy Ophel-Keller (South Australian Research and Development Institute) leads a research group that established the world’s first commercial DNA-based testing service for soilborne diseases (Ophel-Keller et al., 2008). Thus, she has a good knowledge of molecular technologies, and understands the complexities involved in managing beneficial organisms and multiple pathogens in soil. Mike Bell (Queensland Alliance for Agriculture and Food Innovation) provided an agronomic viewpoint. He has worked with tropical and subtropical crops (particularly sugarcane, cereals, peanuts and soybean) for many years, and recognizes that the soil ecosystem must be managed effectively if agriculture is to be productive and sustainable in the long term.

Many other people also contributed by making comments or responding to my queries, and I would like to thank them sincerely. They included Robin Giblin-Davis, Keith Davies, Richard Sikora, Mario Tenuta, Chris Hayward, Alan McKay, Megan Ryan, Nikki Seymour, Richard Humber, Roger Shivas and Emily Rames. Also, a special thank you to Professor David Guest for his support, as the book was compiled while I was an Honorary Associate in the Department of Plant and Food Sciences, Faculty of Agriculture and Environment, The University of Sydney.

I also wish to thank the book production staff at CABI (Rachel Cutts, Alexandra Lainsbury, Laura Tsitildze and their colleagues) for their contribution. They responded quickly to my emails, were always courteous and efficient, and made many helpful suggestions.

My lovely wife, Marcelle, deserves special thanks for her constant support. As a fellow scientist, she understood the time commitment involved in preparing a book of this nature. While I was ensconced in ‘writing mode’, she maintained a home, kept our business operating and was also able to use her artistic talent to prepare Figures 2.6, 3.5, 5.1, 5.2, 5.3, 6.2, 6.4, 8.1, 14.1, 14.2, 14.3 and 14.4. Marcelle, I will be eternally grateful for your help and encouragement.

Finally, I wish to acknowledge the contributions of the nematologists, soil biologists and soil ecologists whose work is cited in this book. Your collective efforts have expanded our knowledge of plant-parasitic nematodes and their natural enemies to the point where biological control now has the capacity to play a crucial role in integrated nematode management programmes.

Graham Stirling

August 2013

Section I

Setting the Scene

1

Ecosystem Services and the Concept of ‘Integrated Soil Biology Management’

Plant-parasitic nematodes are important pests of most of the world’s crops. Estimates of crop loss usually range from 5% to 15%, but higher losses sometimes occur, and there are situations where nematodes are a major factor limiting the production of a particular crop. Although numerous methods are available to either reduce populations of plant-feeding nematodes or enable crops to better tolerate the damage they cause, biological control is generally perceived as playing little or no role in current nematode management programmes. This book will demonstrate that the regulatory mechanisms forming the basis of biological control are actually operating in many agricultural systems (although usually at sub-optimal levels), and that their effectiveness can be enhanced through appropriate management. It argues that modern agriculture must not only be highly productive, but also provide a full range of ecosystem services, including pest and disease suppression; and that this is achievable by incorporating practices into the farming system that increase and sequester carbon, enhance soil biological activity, minimize soil disturbance, improve soil health and ensure long-term sustainability.

Agriculture from an Ecological Perspective

Plants are the lifeblood of all agricultural systems, as they capture energy from the sun and convert it into biomass through the process of photosynthesis. Some of that biomass is then harvested and used to feed and clothe the human population, satisfy the needs of livestock, or provide feedstock for biofuel production. However, what is often forgotten is that plants have many other important roles within agroecosystems: their roots host symbionts that transfer mineral nutrients to the plant, convert atmospheric nitrogen to ammonia, and enhance disease resistance and tolerance mechanisms; plant biomass is the primary source of energy for a decomposer community that breaks down organic matter and recycles nutrients into forms available to plants; and roots, rhizodeposits and plant residues support a complex community of organisms that influence numerous soil physical and chemical properties and also interfere with the pests and pathogens that obtain resources from roots.

The primary role of agriculture is to supply human needs for food and fibre, and in ecological terms this is referred to as a provisioning service (Power, 2010). However, it is clear from the previous paragraph and from Fig. 1.1 that agriculture also provides a range of other important ecosystem services: soil aggregate formation; nutrient cycling; immobilization of nutrients; nitrogen fixation; enhancement of air and water quality; carbon sequestration; detoxification of pollutants, pest control and disease suppression. These supporting and regulating services are provided through the soil biota and are particularly important from an agricultural sustainability and environmental perspective (Powlson et al., 2011a). However, because they are difficult to value in a monetary sense, they are not valued by the agricultural community to the same extent as food and fibre production.

One of the aims of this book is to discuss ways in which soil and plant management practices can be modified so that ecosystem processes within agricultural systems continue to supply provisioning services, but also provide a range of services that support future provisioning. If that goal can be accomplished, one of the outcomes will be a greater level of suppressiveness to plant-parasitic nematodes and other soilborne pathogens.

Biotic Interactions within the Soil Food Web

The community of organisms that live and interact in soil is referred to as the soil food web. The organisms that occupy this food web are dependent on each other for sources of carbon and energy, while the whole biological community is sustained by the photosynthetic activity of plants. Since plants are the primary producers, they form the first trophic level in the soil food web. Primary consumers (bacteria, fungi, plant-feeding nematodes and root-grazing insects) form the second trophic level, as they either feed on living roots or decompose detritus that was originally derived from plants. These organisms then become food and energy sources for higher trophic levels (e.g. bacteria are consumed by nematodes and protozoa; fungal hyphae and spores are eaten by fungivorous nematodes and springtails; and plant-feeding and free-living nematodes are parasitized by fungi or consumed by nematode or arthropod predators). Thus, the soil food web consists of a vast array of interacting organisms that transfer energy from plants to primary and secondary consumers.

Bacteria and fungi are by far the most important component of the soil food web, but many other organisms are also present, including protozoa, nematodes and enchytraeids; a range of microarthropods (e.g. mites, springtails and symphylans); and larger fauna such as termites, millipedes, earthworms, burrowing reptiles and rodents. The main function of the soil food web is to decompose plant material, and mineralize and store nutrients. However, during the decomposition process, soil organisms compete for resources and interact with each other through many different mechanisms, including parasitism, predation, competition and antibiosis. Thus, regulatory forces operating within the soil food web determine the size, composition and activity of the soil biological community and prevent the uncontrolled proliferation of opportunistic organisms. This phenomenon, which is sometimes referred to as ‘biological buffering’ or the ‘balance of nature’, affects all organisms, including nematode pests, and is the basis of biological control.

Fig. 1.1. Impacts of farm management and landscape management on the flow of ecosystem services and disservices to and from agroecosystems. (From Power, 2010, with permission.)

Biological Control of Plant-parasitic Nematodes

The term ‘biological control’ has different meanings to different people. To most farmers, the general public and many pest management consultants, biological control simply means replacing toxic pesticides with safe biological products, a tactic that is often referred to as ‘inundative’ biological control. To some scientists, particularly entomologists and weed scientists, the term refers to what might be termed ‘inoculative’ biological control, where a parasite or predator is deliberately introduced from elsewhere, becomes permanently established in its new environment, and eventually reduces pest populations to acceptable levels. A third form of biological control is not as widely recognized, but is particularly important in soil. It is usually referred to as ‘conservation’ biological control, and involves either providing the resources that endemic natural enemies need to improve their effectiveness, or reducing the factors that are preventing them from being effective parasites or predators. All three forms of biological control apply to nematode pests and are considered in this book.

The essence of biological control is that it encompasses any ecologically based strategy that ultimately results in a reduction in pest populations, or in the capacity of a pest to cause damage. Such effects are manifested through the actions of living organisms and can occur naturally, but may also be achieved by manipulating the soil food web or introducing one or more antagonists. However, when this concept is applied to plant-parasitic nematodes, there is room for debate about whether particular practices should be included under the umbrella term ‘biological control’. For example, nematode populations can be reduced with nematode-resistant crops, and since plants are living organisms, some would consider that resistant plants are ‘biological’ control agents. In the same way, organic amendments may act against nematodes by producing nematicidal by-products or by stimulating natural enemies, and so it is questionable whether the control mechanisms are chemical or biological (see Chapter 9). In yet another example, practices that improve the health of nematode-infested crops through biological processes, but may not reduce nematode populations, are sometimes designated as biological ‘controls’. Since there will always be different views on what is meant by the term, this book focuses on a more important point: that the management practices used in agriculture must be ecologically sound and foster a soil food web capable of keeping populations of plant-parasitic nematodes at levels that do not cause economic damage.

One issue that arises throughout this book is whether the effects of natural enemies in reducing nematode populations should be referred to as ‘control’, ‘suppression’ or ‘regulation’. I have used the latter term to describe situations where populations of a nematode and its parasites or predators respond to each other in a density-dependent manner. Jaffee (1993) described those situations succinctly: ‘when hosts are plentiful, parasites multiply; when parasites are plentiful, hosts are suppressed and parasites then decline’. Although such a model is reasonable when dealing with a single pest and a relatively specific parasite or predator, it is difficult to apply this concept to a complex environment such as soil. Nematodes, for example, are preyed upon by numerous fungi, other nematodes and a wide range of microarthropods, and may also have specific bacterial and fungal parasites. These natural enemies all have different abundances; they are distributed in various micro-niches; they respond to ambient conditions at different rates; they are often in competition; and they may also complement each other. In such a situation, it is difficult to describe these community effects in terms of density-dependent regulation. Thus, I have chosen to refer to this complex soil biotic environment as being suppressive to the pest species.

Due to their widespread use, terms such as ‘biological control’, ‘biocontrol’ and ‘biocontrol agent’ will always be with us. However, the term ‘control’ has connotations of humans being the dominant force, reducing pest populations to low levels with chemicals or other tactics. Suppression seems to be a softer word, and is often used to describe situations where pest populations are reduced through biological processes. It is, therefore, commonly used in this book. Thus, a suppressive soil is one that, due to a multitude of managed or unmanaged biotic and abiotic factors, is not conducive to high pest population levels or exponential multiplication of the pest.

Sustainable Agriculture

The earth’s landscape has been dramatically transformed in the thousands of years since humans began growing crops, but it is still able to produce enough food and fibre to meet the needs of an ever-increasing human population. However, the dependence of modern cropping systems on non-renewable fossil fuels and their role in degrading natural resources and the quality of air, water and soil raises questions about the long-term sustainability of agriculture. Human survival is dependent on the resilience and regenerating capacity of the thin layer of soil covering the earth’s surface, and these attributes are the essence of sustainable agriculture. Not only must our soils produce adequate amounts of food, but they must be farmed in a way that protects their integrity, remediates historical damage and ensures they remain productive for future generations. Thus, the essence of sustainable agriculture is:

the management and utilization of the agricultural ecosystem in a way that maintains its biological diversity, productivity, regeneration capacity, vitality and ability to function, so that it can fulfil – today, and in the future – significant ecological, economic and social functions at the local, national and global level, and does not harm other ecosystems (Lewandowski et al., 1999).

Agricultural sustainability became a major issue for discussion in the latter part of the 20th century due to concerns about the long-term viability of current food production systems (Gliessman, 1984; Pesek, 1989; Edwards et al., 1990; Harwood, 1990; Lal, 1994; Meerman et al., 1996). The prevailing system, characterized by large-scale farms; rapid technological innovation; large capital investments in production and management technology; single crops grown continuously over many seasons; genetically uniform high-yielding crops; extensive use of pesticides and fertilizers; high external energy inputs; dependency on agribusiness; and replacement of farm labour with machinery; has delivered tremendous gains in food production over the last 60 years, but there are questions about the long-term viability of what has been variously termed ‘conventional farming’, ‘modern agriculture’ or ‘industrial farming’ (Gold, 2007). The main concerns are the negative effects on the world’s ecosystems due to soil degradation, water pollution, overuse of surface and ground water, and loss of wetlands and wildlife habitat. Thus, sustainability has become an integral component of the agricultural policies of many countries. Although there are many conflicting views on what elements are, or are not, acceptable and appropriate in a sustainable farming system (Gold, 2007), increasing numbers of farmers are now embarking on their own paths towards sustainability. However, sustainable agriculture should not be seen as a prescribed set of practices. Instead, it is a concept that encourages food producers to reflect on agriculture from an ecological perspective, to think about the long-term implications of their management practices, and then to take steps to redesign or restructure inappropriate farming systems.

Soil Health

Soil, the vital natural resource that sustains agricultural production, is non-renewable and easily ruined by mismanagement. It is continually subject to water and wind erosion; it can be further degraded by compaction and loss of organic matter; and is rendered unproductive by salinization and desertification. Maintaining healthy soil is, therefore, a key component of sustainable agriculture (Jenny, 1984; Doran et al., 1994, 1996; Glanz, 1995; Doran and Safley, 1997). Since soil organisms play a critical role in many important processes associated with soil health (e.g. maintaining soil structure and fertility, cycling nutrients and minimizing pest and disease outbreaks), they are intimately linked with the issue of sustainability. Thus, an important component of sustainable agriculture is the development of soil conservation practices, soil fertility programmes and pest management practices that protect and nurture the organisms responsible for the soil’s long-term stability and productivity.

Although biological attributes (e.g. microbial biomass carbon, soil respiration rate, microbial activity) are commonly used as indicators of soil health, soil organic matter status is arguably the most important parameter determining whether a soil has the capacity to sustain plant productivity and maintain other important soil functions (Powlson et al., 2011a). In fact, the effects of organic matter on soil properties are so far-reaching that they are out of proportion to the relatively small amounts of carbon (0.1–4% w/w) usually found in agricultural soils. The positive impacts of soil organic matter on soil physical, chemical and biological properties are discussed in detail in Chapters 2 and 3, but the role of management in influencing levels of soil organic matter, and its flow-on effects to the soil biological community, is a recurring theme throughout this book.

The Rise of Conservation Agriculture

One of the most important agricultural developments in the last 30 years has been the rise of conservation agriculture (Baker et al., 2006). Defined as an agricultural management system that combines minimum soil disturbance with permanent soil cover and crop rotation, it is the major practical outcome of the recent move towards more sustainable systems of agricultural production. Conservation tillage (a collective term that encompasses a number of commonly used terms, including no-till, direct drilling, minimum tillage and reduced tillage) is a key component of conservation agriculture, and is now practised on more than 95 million hectares of land worldwide (Hobbs et al., 2008). The benefits from conservation tillage are summarized by Hobbs et al. (2008) and discussed more fully in Chapter 4, but include reduced soil compaction, enhanced water infiltration, better moisture retention, improved soil structure, fewer soil losses due to erosion, increased soil organic carbon, higher soil microbial biomass, lower labour costs and fewer inputs of fossil fuels. Conservation tillage, therefore, improves soil health through its effects on soil physical, chemical and biological fertility, and is usually more profitable than farming systems based on conventional tillage. When combined with rotational or cover cropping and retention of plant residues on the soil surface, it provides a farming system that can be used to produce most of the world’s major food and fibre crops, and can be adopted in widely different environments. Given its many advantages and the high rate of adoption in countries such as the United States, Brazil, Argentina, Canada and Australia, conservation agriculture will eventually become the world’s dominant agricultural production system.

Biological Control of Nematodes: Current Status and the Way Forward

Soil fumigants and nematicides were just one of many technological developments during the 1950s and 1960s that resulted in a huge surge in world food production. The sometimes spectacular responses obtained with these chemicals demonstrated that plant-parasitic nematodes were a major constraint to crop production, stimulated scientific and commercial interest in nematodes, and heralded the development of nematology as a discipline. Not surprisingly, biological control was not seen as a high priority during this period. Nematologists concentrated on improving their understanding of the biology, ecology, physiology and taxonomy of this relatively unknown group of pests, while applied research was directed towards maximizing the effectiveness of fumigants and nematicides. Thus, by the time the health and environmental problems associated with the use of nematicides were recognized in the 1980s (Thomason, 1987), research on biological control of plant-parasitic nematodes was still in its infancy and there were ‘no widely accepted examples of the contrived use of an antagonist to control a plant-parasitic nematode’ (Stirling, 1991).

The need to find alternatives to chemical nematicides and decisions in the 1990s to phase out the use of methyl bromide because of its ozone-depleting properties (Ristaino and Thomas, 1997) provided compelling reasons to add biological control to the range of tools available to manage nematode pests. Mainstream research programmes in nematology were modified to include biological control, and scientists with an interest in the natural enemies of nematodes were employed by many research agencies. Thus, biological control became one of the main growth areas in nematology, with biological control and resistance being the only two subject areas where the number of papers published in the Journal of Nematology more than doubled in the years since 1979 (Fig. 1.2).

Although an infusion of resources into biological control has increased our understanding of the way nematodes and their antagonists interact in soil, it is often argued that this change in the focus of nematological research has produced relatively little in terms of practical outcomes. Biological control is rarely recognized as a component of current nematode management programmes, and so it is reasonable to ask why. I would argue that this situation has developed because biological control is usually viewed in a very limited sense as replacing a chemical pesticide with a biological alternative (i.e. replacing one ‘silver bullet’ with another). There is certainly evidence to suggest that such an approach is sometimes useful, as several biological products with activity against nematodes are now available in the marketplace (see Chapter 12). However, the use of inoculants in mainstream nematode management programmes will always be hampered by economic limitations and biological constraints. In many agricultural situations, it is not feasible to mass produce an antagonist, transport it to the required location, and incorporate it into soil at the application rates required to achieve useful levels of nematode control; while the buffering effects of the microbial community inevitably operate against the biological control agent once it is introduced into soil. The alternative approach of manipulating the farming system, the environment or the host plant to achieve a soil biological community capable of suppressing nematode pests is, therefore, the major focus of this book. It is based on the proposition that wherever agriculture is practised, the requisite components of the soil food web will already be present and adapted to local conditions. The challenge is to redesign management practices to enhance their activity.

Fig. 1.2. Changes in the level of activity within various areas of nematology over four decades, as determined by the percentage of papers published in Journal of Nematology. (Figure prepared from data presented by McSorley, 2011a, and published with permission.)

Integrated Soil Biology Management

The main reason that plant-parasitic nematodes are important crop pests is that much of the land currently used for agriculture has been exploited for many years and is physically, chemically and biologically degraded. The regulatory mechanisms that normally suppress nematode populations no longer operate as they should, while a sub-optimal physical and chemical environment means that plants are unable to tolerate the damage nematodes cause to their root systems. Thus, excessive fertilizer and pesticide inputs are required to maintain production, further weakening an already depleted soil biological community. Given that carbon levels in agricultural soils are almost always more than 50% lower than undisturbed soils in their natural state; that soil organic matter plays a central role in improving a soil’s physical, chemical and biological properties; and that improvements in soil health result from interactions between occupants of the detritus-based food web; the ultimate solution is to focus on building an active and diverse biological community by increasing carbon inputs, minimizing carbon losses and reducing management impacts on soil organisms. The advantage of this approach is that it targets the primary cause of the nematode problem (management-induced diminution of the soil biota and shortcomings in the farming system) rather than the secondary effect (the presence of a nematode community dominated by plant parasites). Improved soil health and enhanced sustainability will be the most important outcomes of such an approach, but biological mechanisms that suppress nematodes will also be activated. Other outcomes are likely to be broad-spectrum suppression of other root pathogens and an increased capacity of crops to tolerate the effects of these pathogens.

The important point in the preceding paragraph is that the management practices required to enhance soil biological activity and diversity are the foundation on which effective systems of minimizing losses from plant-parasitic nematodes can be built. This argument is based on the premise that once crop rotation and cover cropping become integral components of the farming system, cropping frequency is increased; bare fallows are eliminated; tillage is minimized; crop residues are retained on the soil surface; levels of soil organic matter are raised; compaction and other sub-optimal soil constraints are removed; inputs of nutrients are optimized; and pesticides are used judiciously, then biological control mechanisms will begin to operate effectively, and will provide enhanced levels of nematode suppression. Evidence that this occurs is presented throughout this book.

The advantage of this approach is that the focus is no longer on the pest. Instead, the focus is on fostering the biological resources that must be in place if the agroecosystem is to provide the full range of ecosystem services depicted in Fig 1.1. It is, therefore, a wider concept than integrated pest management (IPM), an approach that is commonly used to minimize damage caused by insect pests, weeds, plant pathogens and nematodes. It has been termed ‘integrated soil biology management’ in this book, and it aims to build an active and diverse soil biological community that will not only suppress nematode pests but also improve the soil’s physical properties, enhance biological nutrient cycling and provide the many other services provided by the soil biota. As discussed in Chapter 11, some of the tactics used in IPM approaches to managing nematodes are incompatible with the concept of integrated soil biology management, or are of questionable value (see Table 11.2). The two approaches are, therefore, quite different. Integrated soil biology management has a pest-management component, but is really an integrated approach to managing soil biological resources with a view to promoting sustainable and productive agriculture. Thus, it has similarities to some of the approaches discussed in a workshop on soil management sponsored by the Food and Agriculture Organization of the United Nations (FAO) in 2002 (FAO, 2003).

In some cropping systems and environments, serious nematode pests of the principal crop may not be present, and so when sustainable soil and crop management systems are being developed, it is not necessary to include tactics that target particularly damaging nematode species. Improving soil health and enhancing suppressiveness to soil-borne pests may be all that is required to minimize losses from plant-parasitic nematodes. However, in situations where a virulent nematode is capable of causing crop losses at low population densities, management tactics directed at that pest (e.g. a resistant/tolerant cultivar or rootstock, or a non-host rotation crop) will be an important component of any management system that is devised.

One potential problem with management systems that aim to enhance suppressiveness to plant-parasitic nematodes is that in many agricultural soils, the predatory component of the soil food web may already have been eliminated or severely depleted by many years of mismanagement. In such situations, remediation measures are likely to be needed, and it may take many years to restore a fully functional soil biological community. The challenges involved in tackling these issues are discussed in Chapter 11.

Transferring Ecological Knowledge into Practical Outcomes

The key message from this introductory chapter is that agroecosystems should be managed with two principal aims in mind: to sustain long-term plant productivity, and to maintain a full range of ecosystem services. Thus, any practice that is integrated into the system in an attempt to reduce losses from plant-parasitic nematodes must be considered holistically, and should recognize the following:

• The primary goal of management must be to establish a farming system that protects the soil resource from degradation; enhances rather than diminishes soil carbon levels; increases soil microbial activity; enhances biological diversity; and is productive and sustainable in the long term. Any practice that is used to manage nematodes must be compatible with these goals.

• Nematode management practices must have a sound ecological basis. Plant-parasitic nematodes are only one component of a complex biological community, and tactics used to reduce their population densities should not diminish the capacity of the wider community to fulfil its functions.

• Reducing populations of plant-parasitic nematodes to low levels may not always be necessary. In a well-functioning agro-ecosystem, the soil health benefits associated with improved physical and chemical fertility may increase damage thresholds to the point where the crop suffers minimal losses, despite the presence of plant-feeding nematodes.

The primary purpose of this book is to consider how our knowledge of the soil ecosystem can be used to reduce losses from plant-parasitic nematodes. It commences with three chapters that explore the links between the soil biological community, soil health and sustainable agriculture (Chapters 2–4). The natural enemies of nematodes and the symbionts that have the capacity to kill nematodes or interfere in some way with their development are then discussed (Chapters 5–8), and examples demonstrating that these antagonists can suppress populations of plant-parasitic nematodes are given in Chapters 9 and 10. The management practices required to conserve and enhance natural enemies of nematodes are considered in Chapter 11, while recent progress with inundative biocontrol is reviewed in Chapter 12. The main points made in the book are summarized in Chapter 13, and the many important issues that require further research are also discussed. Chapter 14 is a practical guide to improving soil health. It is written for land managers and their direct advisors in the hope that it will encourage them to improve the sustainability of their farming systems and introduce practices that enhance the suppressiveness of their soils to plant-parasitic nematodes.

Given the broad range of topics that are covered (the soil environment, the soil food web, the nematode community and soil ecosystem management within sustainable agriculture), it is important to appreciate that the segments of this book are not designed to stand alone. The soil biological community is complex; organisms within the soil food web interact with plants and with each other; both plants and the soil biota are affected by the soil environment; and options for managing agroecosystems depend on the soil resource, climate, the principal crop and many other factors. Thus, to gain a holistic view of the main messages, it is necessary to read the entire book.

Section II

The Soil Environment, Soil Ecology, Soil Health and Sustainable Agriculture

2

The Soil Environment and the Soil–Root Interface

Any discussion of biological control of plant-parasitic nematodes would be incomplete without some consideration of the soil environment. Plant-parasitic nematodes spend most of their lives in soil, but since they also develop an intimate relationship with roots during the feeding process, it is perhaps more correct to consider them as occupying the soil–root interface rather than the bulk soil mass. Eggs of some plant-parasitic nematodes hatch in response to substances that diffuse from roots, and feeding takes place in non-suberized areas of the root system near root tips and root hairs, and in regions where lateral roots emerge. The bodies of ectoparasitic nematodes remain in the thin layer of soil no more than 2 mm thick surrounding the root; adult females of some sedentary endoparasites protrude into this zone; and the eggs of many species are aggregated on the root surface. Such distinctions about the habitat of plant-parasitic nematodes may seem trivial but they are vitally important when population regulation and biological control are considered. Essentially, biological control is concerned with interactions between pests and antagonists and it is important to define the battlefield where this ‘biological warfare’ occurs. During fallow periods between host crops, this battlefield is localized microsites within the bulk soil mass. However, once a crop is planted, plant-parasitic nematodes aggregate near roots, and so biological control agents must be effective at the soil–root interface.

In introductory remarks to his book on soil biology, Bardgett (2005) argued that the first step in understanding the factors that control the abundance and activity of soil organisms and cause spatial and temporal variability within soil biological communities is to understand the physical and chemical matrix in which they live. However, that is not as simple as it may seem, because soil physical and chemical properties not only affect soil biological activity, but are also modified by the organisms that reside in soil. Thus, soil is a complex and dynamic medium, and its final state is the result of numerous interactions between its mineral fraction, organic matter and the soil biota. Plants, microorganisms and the soil fauna play a key role in soil formation and influence many important soil properties. Consequently, the first part of this chapter concentrates on the biologically inert components of soil, the process of soil formation, and the soil physical and chemical parameters that influence soil organisms. It then discusses the effects of organic matter on soil properties and the critical role of plant roots in harbouring soil organisms and influencing soil properties. Further information on these matters can be found in various texts on soil science and soil biology, including Coleman and Crossley (2003), Davet (2004), Bardgett (2005), Sylvia et al. (2005), Lavelle and Spain (2005), Uphoff et al. (2006), White (2006), van Elsas et al. (2007a), Brady and Weil (2008), Chesworth (2008) and Tan (2009).

The Process of Soil Formation and the Composition of Soil

The soil mineral fraction

Soil is the result of weathering processes that have operated over millions of years to break down the parent rock into smaller and smaller particles. Thus, the mineralogical composition of the parent material influences the types of soils that are formed and the character of the vegetation they support. The original parent material, temperature, the amount of precipitation in the region where the soil developed and the time involved in the soil-formation process all affect soil texture (the proportion of sand, silt and clay), and this in turn has a major impact on many important soil properties. The coarser sand and silt fractions are comparatively inert, because the surface area of the particles is small relative to their weight, and their capacity to retain cations is negligible. Therefore, sand and silt particles do not readily retain water, nutrients and humic substances, and do not support a high proportion of the indigenous microbial population. Their main role is to enhance the porosity of fine-textured soils, improve the propensity of a soil to drain water and facilitate water and gas diffusion.

From a biological perspective, clays are by far the most important inert constituent of soil for several reasons:

• The negative charge on the surface of clay particles confers a capacity to buffer pH changes. H+ ions can be exchanged for other cations, and this helps organisms that are present in the liquid phase to withstand sudden changes in pH.

• Reversible electrostatic bonds that are formed between clays and positively charged particles confer the ability to retain and exchange cations. This property (known as the cation exchange capacity) is of vital importance to plant growth and has direct and indirect effects on soil organisms.

• Clay soils are capable of storing large quantities of water. Thus, in climates where rainfall is variable or limited, moisture conditions favour biological activity for much longer in soils with moderate to high clay contents than in coarse-textured soils.

• Clays not only retain mineral ions, but also organic molecules. In clay soils, organic substances are often held within microaggregates and are, therefore, temporarily protected from degradation by microorganisms and soil enzymes, ensuring the slow release of some of the soil’s nutrient reserves.

Soil organic matter

Although the mineral fraction is by far the dominant component of soil, the organic fraction (which usually comprises only 1–4% of the weight of most agricultural soils), is the key factor influencing the soil biota and a major determinant of soil properties. However, most routine analytical methods for measuring soil organic matter (SOM) actually determine the content of soil organic carbon (SOC). Conversion factors that account for the proportion of SOM that is not carbon are then applied to obtain SOM contents. These conversion factors range from 1.7 to 2.0, but a factor of 1.72 is typically used (i.e. SOM = SOC × 1.72). Since no single conversion factor is appropriate for all soils, it is now more common to report results in terms of SOC (Baldock and Skjemstad, 1999).

Soil organic carbon contents vary enormously between soils and also within a specific soil type (Fig. 2.1), due largely to differences in the major soil-forming factors (climate, soil mineral composition, topography, vegetation and soil biota), and the way a soil is managed by humans. In natural systems, the amount of soil organic carbon tends towards an equilibrium that is determined by the rates of carbon inputs and losses, but in agricultural soils, continual changes in management and cropping practices result in levels of soil organic carbon that are in a continual state of flux. However, if management practices remain consistent for long enough (20–50 years?), it is possible for an agricultural soil to attain an average equilibrium value that reflects the rotation or suite of management practices imposed.

Fig. 2.1. Variability in soil organic carbon between major soil groups in Australia, and within specific soil types. Values (median and quartile ranges) are expressed in SI units but can be converted to the percentage values traditionally used to measure soil organic carbon by dividing by 10. (Modified from Baldock and Skjemstad, 1999, with permission.)

Soil organic matter is derived from plants, the primary producers in all ecosystems, as they convert energy from the sun and carbon from the atmosphere into organic molecules and living tissues. Thus, the primary organic inputs into soil are leaves and twigs that fall to the ground; dead roots; cells that are sloughed from roots; carbohydrates, proteins and other substances that are exuded from roots; and carcasses and wastes from all the animals that feed on plants. This detritus is then subject to microbial decomposition. Labile compounds (e.g. sugars and proteins) are the first to decompose, and then the more resilient materials (which largely consist of cellulose and lignin) are converted into a complex range of polysaccharides, polypeptides and organic acids. As this process continues, detritus is progressively transformed into complex and relatively recalcitrant molecules known as humus. Thus, soil organic matter consists of a number of components that vary in physical size, chemical composition, degree of association with soil minerals and extent of decomposition. These components are depicted in Fig. 2.2 and comprise: (i) living biomass (microorganisms, larger soil organisms and intact plant and animal tissues); (ii) organic materials in the soil solution; (iii) particulates (roots and other recognizable plant residues); (iv) humus (a largely amorphous and colloidal mixture of organic substances that are no longer identifiable as plant or animal tissues); and (v) inert organic materials such as charcoal.

Fig. 2.2. A definition of soil organic matter and descriptions of its various components. (From Baldock and Skjemstad, 1999, with permission.)

Inputs of organic matter are particularly important in soil profile development. Litter deposited on the soil surface, organic materials derived from roots and the biological activity associated with roots and detritus produce soils with a layered structure. The litter layer and the organic horizon immediately beneath it are the most biologically active layers in the soil profile, as they are largely composed of fresh plant material and organic matter in various stages of decomposition. The uppermost mineral layer (A horizon) is also vitally important, as it contains humified organic material and organic matter derived from above. Collectively, these surface layers, which are usually no more than 10–15 cm deep, are the most functionally important zones in the soil profile, as they determine a soil’s capacity to respond to environmental stresses and carry out ecosystem functions.

Soil organic matter is composed of several carbon fractions that vary in their turnover times or rate of decomposition. The labile fraction, which turns over in less than 5 years, is the primary food source for soil microorganisms, and since fungal hyphae and bacterial mucilages play a major role in binding soil particles into microaggregates, labile carbon is particularly important in influencing soil physical properties. It is also important from a chemical perspective, because nutrient cycling in soil is largely associated with the organisms involved in decomposing labile compounds from plant residues and root exudates.

The humic fraction is also a significant contributor to soil chemical and physical properties. This fraction is a mixture of large, amorphous, colloidal, dark-coloured polymers with aromatic, ring-type structures (e.g. fulvic acids, humic acids and humins) and comprises about 50–80% of soil organic matter. These substances are remarkably resistant to microbial degradation, with fulvic acid surviving unchanged in soil for decades and more recalcitrant materials having half-lives that are measured in centuries. Nevertheless, humus is subject to limited but continual microbial attack and so recurring additions of plant residues are required to maintain levels