CABI in Review 2014 Ebook

CABI in review14 Selected book chapters For our annual review this year, we have made available selected chapters from CABI books in a CABI in Review 2014 eBook. The chapters have been taken from the following books (click on the book to take you directly to that chapter).

Click here for more information about our work in Knowledge and Publishing This chapter is from the book: 9781780644158.pdf

ISBN: 9781780644158 Contents

Foreword xv Preface xix Acknowledgements xxiii

SECTION I SETTING THE SCENE 1 Ecosystem Services and the Concept of ‘Integrated Soil Biology Management’ 3 Agriculture from an Ecological Perspective 3 Biotic Interactions within the Soil Food Web 4 Biological Control of Plant-parasitic Nematodes 5 Sustainable Agriculture 6 Soil Health 7 The Rise of Conservation Agriculture 7 Biological Control of Nematodes: Current Status and the Way Forward 7 Integrated Soil Biology Management 9 Transferring Ecological Knowledge into Practical Outcomes 10

SECTION II THE SOIL ENVIRONMENT, SOIL ECOLOGY, SOIL HEALTH AND SUSTAINABLE AGRICULTURE 2 The Soil Environment and the Soil–Root Interface 15 The Process of Soil Formation and the Composition of Soil 16 The soil mineral fraction 16 Soil organic matter 16 Impact of Organic Matter on Soil Properties 19 Organic matter and soil physical fertility 19 Organic matter and soil chemical fertility 21 Organic matter and soil biological fertility 22 The Soil Environment and Its Impact on Nematodes and Other Soil Organisms 23 Physical structure 23

v vi Contents

Soil water 24 Aeration 25 pH 26 Soil temperature 27 The Soil–Root Interface 27 Roots and rhizodeposits: the energy source that sustains the soil biological community 28 Microbial inhabitants of the soil and rhizosphere 32 Microbial colonization of the rhizosphere 34 Communication within the rhizosphere 35 Plant–microbe–faunal interactions in the rhizosphere 36 Effects of rhizosphere inhabitants on plant growth 40 Manipulating the rhizosphere community 41 Implications for Biological Control 43 Impact of the soil environment 43 Multitrophic interactions in a complex environment 44 The soil and rhizosphere as a source of antagonists 45 Establishment of biological control agents in soil and the rhizosphere 46 Manipulating the soil biological community 46 The role of organic matter 47 3 The Soil Food Web and the Soil Nematode Community 48 Major Groups of Organisms in Soil 48 Microbiota 49 Microfauna 49 Mesofauna 50 Macrofauna 50 Structure of the Soil Food Web 50 Impact of Land Management on Energy Channels within the Soil Food Web 52 Interactions within the Soil Food Web 55 Regulation of Populations by Resource Supply and Predation 56 Impacts of the Soil Food Web on Ecosystem Processes: Storage and Cycling of Nutrients 57 The Soil Nematode Community 59 Trophic groups within the soil nematode community 59 A functional guild classification for soil nematodes 62 Ecological roles of free-living nematodes 62 Microbial feeding 63 Microbial transport 65 Nutrient cycling 65 Regulation of populations 66 Plant-parasitic nematodes 67 Major groups of plant-feeding nematodes and their economic impact 67 Population dynamics and damage thresholds 70 Implications for Biological Control 71 The role of the soil food web and the soil environment 71 Major crops and nematode pests: their relevance to biological control 72 Endoparasitic nematodes as a target for biological control agents 74 Sedentary endoparasites 74 Migratory endoparasites 75 Features that protect plant-parasitic nematodes from parasitism and predation 76 Contents vii

4 Global Food Security, Soil Health and Sustainable Agriculture 77 Global Food Security 77 Sustainable Farming Systems 78 Sustainable agricultural intensification 79 Reduced tillage 79 Continual cropping and maintenance of a permanent cover of plant residues 79 Greater plant diversity 80 Improved crop yield potential 80 Optimized crop nutrition 80 Efficient water management 81 Site-specific management 81 Integrated pest management 81 Integrated crop and livestock production 81 Soil Health 81 Management impacts on soil health and the role of conservation agriculture 82 Other management practices to improve soil health 83 Well-adapted, high-yielding varieties 83 Optimal nutrient management 84 Efficient water management 84 Integrated pest management 85 Variable-rate application and site-specific management 85 Integrated crop and livestock production 85 Ecologically sound management systems: the pathway to healthy soils 86 Soil-health benefits from conservation agriculture and precision farming: Australian examples 86 Indicators of soil health 88 Ecological Knowledge, Biotic Interactions and Agricultural Management 90 Management effects on the soil biota and the limiting role of the environment 91 Provision of ecosystem services by the soil biota and the role of management 92 Integrated Soil Biology Management 93 Ecologically Based Management Systems and the Role of Farmers 95 Implications for Biological Control 96

SECTION III NATURAL ENEMIES OF NEMATODES 5 Nematophagous Fungi and Oomycetes 101 Taxonomy, Infection Mechanisms, General Biology and Ecology 102 Nematode-trapping fungi in the order Orbiliales 102 Trapping structures 102 Taxonomy 103 Occurrence 105 General biology and ecology 106 Fungal and oomycete parasites of vermiform nematodes 106 Stylopage 106 Catenaria 106 Nematoctonus, Hohenbuehelia and Pleurotus 108 Drechmeria 108 Harposporium 109 Hirsutella 111 viii Contents

Nematophagous oomycetes: Myzocytiopsis, Haptoglossa, Nematophthora and Lagenidiaceae 113 Cyst and egg parasites 115 Pochonia 115 Purpureocillium 119 Brachyphoris, Vermispora and the ARF fungus 123 Other fungi 124 Fungal–Nematode Interactions in Soil 127 Saprophytic and parasitic modes of nutrition 127 Factors influencing the saprophytic and parasitic activity of nematophagous fungi in soil 127 Density-dependent response as nematode populations increase 127 Competition from other soil organisms for nutrients 128 Competition for nitrogen in high-carbon, low-nitrogen environments 130 Nematophagous Fungi as Agents for Suppressing Nematode Populations 131 Occurrence in agricultural soils 131 Population density and predacious activity in soil 132 The regulatory capacity of nematophagous fungi 136 Endoparasitic fungi 137 Nematode-trapping fungi 138 Cyst and egg parasites 139 Host specificity within the nematophagous fungi 139 Interactions between nematophagous fungi and nematodes in the rhizosphere 140 Association of nematode-trapping and endoparasitic fungi with roots 141 Rhizosphere competence of fungi and oomycetes capable of parasitizing nematode cysts and eggs 141 Nematophagous fungi and entomopathogenic nematodes 142 Citrus root weevil, entomopathogenic nematodes and nematophagous fungi in citrus soil 143 Moth larvae, entomopathogenic nematodes and nematophagous fungi in natural shrub-land soil 144 The impact of organic matter on predacious activity 146 Other factors influencing predacious activity 150 Maximizing the Predacious Activity of Nematophagous Fungi in Agricultural Soils 152 6 Nematodes, Mites and Collembola as Predators of Nematodes, and the role of Generalist Predators 157 Predatory Nematodes 157 Characteristics of the five major groups of predatory nematodes 158 The prey of predatory soil nematodes 159 Predatory nematodes as regulatory forces in the soil food web 163 Impacts of agricultural management on omnivorous nematodes and generalist predators 164 Short- and long-term effects of soil fumigation 164 Negative effects of other agricultural management practices 165 Management to maintain a well-structured soil food web 167 Maintaining the suppressive services provided by predatory nematodes and other generalist predators 170 Predatory nematodes and inundative biocontrol 171 Microarthropods as Predators of Nematodes 171 The main members of the soil mesofauna: mites, Collembola and Symphyla 171 Contents ix

Evidence of nematophagy in various groups of microarthropods 172 Results from field observations, feeding studies and analyses of gut contents 172 Detection of predation using stable isotope ratios and molecular techniques 174 Studies of ‘fungivorous’ and ‘predatory’ arthropods in microcosms 175 Mesostigmata as predators of nematodes in agroecosystems 177 Management to enhance microarthropod abundance and diversity in agricultural soils 178 Miscellaneous Predators of Nematodes 181 Generalist Predators as Suppressive Agents 182 Concluding Remarks 185 Generalist predators as indicators of ecological complexity and a capacity to suppress pests 185 Conservation (or autonomous) biological control 186 Practices associated with developing self-regulating agroecosystems 188 The disconnect between agricultural scientists, soil ecologists and the farming community 188 7 Obligate Parasites of Nematodes: Viruses and Bacteria in the Genus Pasteuria 193 Viral Infectious Agents of Nematodes 193 Bacteria in the Genus Pasteuria 194 Distribution, host range and diversity 194 Taxonomy, systematics and phylogeny 194 Pasteuria penetrans: A Parasite of Root-knot Nematodes (Meloidogyne spp.) 196 Life cycle and development 196 Pathogenicity, pathogenesis and the impact of temperature 198 Host specificity 199 Estimating endospore numbers in soil 200 The interaction between P. penetrans and its nematode host in soil 201 Endospore production and release into soil 202 The impact of the physical and chemical environment on endospores, and on the spore-attachment process 202 Impact of spore concentration on nematode infectivity and fecundity 204 Miscellaneous factors influencing the production and survival of endospores in soil 208 The potential of P. penetrans as a biological control agent 209 Pasteuria as a Parasite of Cyst Nematodes (Heterodera and Globodera spp.) 210 Taxonomy, phylogeny and host specificity 210 Ecology and biological control potential 211 Candidatus Pasteuria usgae Parasitic on Sting Nematode (Belonolaimus longicaudatus) 212 Taxonomy and host specificity 212 Ecology and biological control potential 213 Commercial products created by in vitro culture 216 Pasteuria as a Parasite of Other Plant-parasitic and Free-living Nematodes 216 Parasitism of root-lesion nematodes (Pratylenchus spp.) by Pasteuria thornei 216 Parasitism of citrus nematode (Tylenchulus semipenetrans) by Pasteuria 217 An isolate of Pasteuria parasitizing a reniform nematode (Rotylenchulus reniformis) 218 x Contents

Density-dependent parasitism of Xiphinema diversicaudatum by Pasteuria 218 Associations between Pasteuria and other nematodes 219 Concluding Remarks 220

SECTION IV PLANT–MICROBIAL SYMBIONT–NEMATODE INTERACTIONS 8 Arbuscular Mycorrhizal Fungi, Endophytic Fungi, Bacterial Endophytes and Plant Growth-promoting Rhizobacteria 225 Arbuscular Mycorrhizal Fungi 225 Benefits to plants from a symbiotic relationship with arbuscular mycorrhizal fungi 226 Enhanced nutrient uptake 226 Drought tolerance 227 Improved soil structure 227 Disease resistance 227 Interactions between plants, arbuscular mycorrhizal fungi and plant-parasitic nematodes 228 Management to enhance arbuscular mycorrhizal fungi 231 Reduced tillage 231 Fallow management, cropping intensity, crop sequence and cover cropping 231 Other crop and soil management practices 232 Improving soil and plant health, and managing nematodes with arbuscular mycorrhizal fungi 233 Endophytic Fungi 234 Grass endophytes 235 Fusarium endophytes 236 Nematode control with endophytic strains of Fusarium oxysporum 236 Approaches to utilizing Fusarium-mediated resistance to plant-parasitic nematodes 238 Endophytic nematophagous fungi 239 Concluding remarks on fungal endophytes: moving into uncharted waters 239 Bacterial Endophytes and Rhizosphere-inhabiting Bacteria 239 Mechanisms associated with growth promotion by rhizobacteria 240 Provision of nutrients 241 Production of plant growth regulators 241 Suppression of soilborne pathogens 241 The impact of plant growth-promoting rhizobacteria on plant-parasitic nematodes 241 Interactions between rhizosphere- and root-inhabiting bacteria and plant-parasitic nematodes 244 Mechanisms by which root-associated bacteria influence plant-parasitic nematodes 245 Production of bioactive compounds 245 Chitinolytic, proteolytic and lipolytic activity 246 Induction of systemic resistance 248 Manipulating populations of rhizobacteria for nematode management 249 Impact of crop rotation, organic amendments and other practices 249 Root-associated Symbionts: Only One Component of the Rhizosphere Microbiome 250 Contents xi

SECTION V NATURAL SUPPRESSION AND INUNDATIVE BIOLOGICAL CONTROL 9 Suppression of Nematodes and Other Soilborne Pathogens with Organic Amendments 255 Organic Matter-mediated Suppressiveness for Managing Soilborne Diseases 256 Sources of organic matter for use as amendments, and their beneficial effects 256 Impact of organic source and application rate on disease suppression 258 Effects on pathogen populations and disease 259 Variation in responses to organic inputs 259 Mechanisms of action 260 Indicators of broad-spectrum disease suppressiveness 260 Organic Matter-mediated Suppressiveness to Plant-parasitic Nematodes 262 Soil fertility and plant nutrition effects of organic amendments 264 Nematicidal compounds from decomposing organic matter 265 Pre-formed chemicals in plant materials 265 Chemicals released during the decomposition process 266 The contribution of phytochemicals to the nematicidal effects of organic amendments 267 Nematicidal properties of nitrogenous amendments 268 Enhancing biological control mechanisms with organic amendments 269 Impact of amendments on natural enemies, particularly nematophagous fungi 269 The capacity of different types of organic matter to enhance biological mechanisms of nematode suppression 271 Amendments with a high C:N ratio: are they the key to more sustained suppressiveness? 273 Temporal effects of amending soil with organic matter 275 Incorporation of amendments versus mulching 275 The way forward: combining multiple mechanisms of action 277 10 Specific Suppression of Plant-parasitic Nematodes 280 The Role of Fungi and Oomycetes in the Decline of Heterodera avenae 280 Parasitism of Meloidogyne spp. on Peach by Brachyphoris oviparasitica 286 Suppression of Heterodera schachtii by Brachyphoris oviparasitica and Other Fungi 287 Parasitism of Mesocriconema xenoplax and Heterodera spp. by Hirsutella rhossiliensis 288 Decline of Heterodera glycines and the Possible Role of Egg-parasitic Fungi 290 Suppression of Root-knot Nematode by Pochonia chlamydosporia and Other Organisms 292 Suppression of Heterodera glycines and Sudden Death Syndrome of Soybean 293 Suppression of Root-knot Nematodes by Pasteuria penetrans 294 Suppression of Heterodera glycines by Pasteuria nishizawae 297 Management Options to Enhance Specific Suppressiveness 298 The role of tolerance, resistance and crop rotation 298 The impact of tillage 300 Integrated management to improve the efficacy of Pasteuria 300 Making Better Use of Natural Control: The Way Forward 301 xii Contents

11 Integrated Soil Biology Management: The Pathway to Enhanced Natural Suppression of Plant-parasitic Nematodes 304 Assessing Soils for Suppressiveness to Plant-parasitic Nematodes 305 Survey methods to identify nematode-suppressive soils 305 Bioassays for suppressiveness 306 Indicators of suppressiveness 306 Modifying Farming Systems to Enhance Suppressiveness 308 Organic Matter Management: The Key to General Suppressiveness 309 Management impacts on soil carbon, and flow-on effects to the soil biota 309 Tillage and its impact on suppressiveness 312 Using organic amendments, cover crops and mulches to enhance suppressiveness 313 Impact of Management on Specific Suppressiveness 314 Integrated Nematode Management or Integrated Soil Biology Management? 315 Integrated Soil Biology Management in Various Farming Systems: The Pathway to Enhanced Suppressiveness 317 Grains, oilseeds, pulses, fibre crops and pastures 318 The key role of conservation agriculture 318 Integration of pastures into crop-based farming systems 320 Impact of management on soil biological parameters 322 Vegetable crops 324 Organic amendments 325 Crop rotation, cover cropping and other practices 325 Integrated management 326 Perennial crops 328 Enhancement of general suppressiveness 330 Enhancement of specific suppressiveness 331 An example of progress: nematode-suppressive soils in sugarcane 332 Organic farming systems 335 Impediments to the Development and Adoption of Farming Systems that Improve Soil Health and Enhance Suppressiveness 337 Sustainable Weed Management Systems for Minimum-till Agriculture: A Priority for Research 338 The Way Forward: A Farming Systems Approach to Managing Nematodes 339 12 Biological Products for Nematode Management 342 Experimental Methods 343 General Soil Biostasis and the Fate of Introduced Organisms 344 Monitoring Introduced Biological Control Agents 348 Commercial Implementation of Biological Control 350 Inundative Biological Control of Nematodes: An Assessment of Progress with a Diverse Range of Potentially Useful Organisms 351 Nematode-trapping fungi 351 Endoparasitic fungi 358 Cyst and egg parasites 360 Pochonia 360 Purpureocillium 362 Trichoderma 367 Other fungi 368 Pasteuria 370 Contents xiii

Predatory and entomopathogenic nematodes, and microarthropods 375 Plant growth-promoting rhizobacteria and endophytes 377 Rhizobacteria and bacterial endophytes 377 Arbuscular mycorrhizal fungi 379 Fusarium endophytes 381 Combinations of Biocontrol Agents 383 The Role of Organic Amendments in Enhancing the Performance of Biological Products for Nematode Control 385 Inundative Biological Control as a Component of Integrated Nematode Management 386 Summary and Conclusions 387

SECTION VI SUMMARY, CONCLUSIONS, PRACTICAL GUIDELINES AND FUTURE RESEARCH 13 Biological Control as a Component of Integrated Nematode Management: The Way Forward 393 Ecosystem Services Provided by the Soil Biological Community, and the Key Role of Organic Matter 394 Farming Systems to Improve Soil Health and Sustainability 394 Will Suppressiveness be Enhanced by Modifying the Farming System? 395 The impact of plant residues, root exudates and other sources of organic matter on natural enemies of nematodes 395 The role of continual cropping and increased cropping intensities 396 Reducing tillage results in multiple benefits that will improve soil health and enhance suppressiveness 397 The Role of Inundative and Inoculative Biological Control 398 Moving from Theory to Practice: Issues Requiring Attention 398 Assessment of suppressive services in long-term trials 399 Relationships between soil carbon status, biological activity, biodiversity and general suppressiveness 400 Management of specific suppressiveness 400 Understanding interactions between the nematode community, natural enemies and organic matter 401 Food preferences of parasites and predators in the soil environment 402 Improved monitoring and diagnostic services for nematode pests and their natural enemies 403 Coping with biological complexity 403 Multidisciplinary research, innovation networks, research/extension models and the role of farmers 404 The efficacy of inundative biological control in complex and dynamic soil environments 405 Concluding Remarks 406 14 A Practical Guide to Improving Soil Health and Enhancing Suppressiveness to Nematode Pests 408 Sustainable Agriculture and its Ecological Basis 408 Biological communities and ecosystem services 408 Soil biological communities 409 The soil food web 409 Soil physical and chemical fertility, and the role of organic matter 412 xiv Contents

Soil fertility decline and the impact of management 413 Excessive tillage 413 Inadequate residue management 414 Excessive fertilizer and pesticide inputs 414 Soil compaction 414 Sustainable farming systems 414 A Guide to Improving Soil Health and Minimizing Losses from Soilborne Diseases 415 Step 1. Assess soil health 415 Step 2. Assess impacts of the farming system on soil health and consider options for improvement 415 Step 3. Modify soil and crop management practices and assess the outcomes 416 Biological Control of Nematodes: One of Many Important Ecosystem Services 417 Nematode-suppressive soils 418 Nematode Management within Sustainable Farming Systems 420 Examples of potentially sustainable farming systems 420 Large-scale production of grains, oilseeds, fibre crops and pastures 420 Vegetable crops 421 Perennial trees and vines 422 Other crops 423 Indicators of improvement 423 Potential problems and possible solutions 424 Conclusions 424 Questions Related to Soil Health, Soil Organic Matter and Nematode Management 425 Useful Information on Soil Health 427

References 429 Index of Soil Organisms by Genus and Species 495 General Index 501 4 Global Food Security, Soil Health and Sustainable Agriculture

The decision to commence this book with a production has increased to an even greater broad overview of the many issues likely to extent, markedly decreasing the proportion affect the development of biological controls for of malnourished people in the world. New plant-parasitic nematodes was deliberate. The livestock and crop production technologies complexity of the soil environment; the diversity have enabled food to be produced in ways of agricultural production systems; and the that would never have been contemplated by sheer number of economic and production- previous generations of farmers. However, related issues that must be considered by today’s world population is expected to reach 9 bil- food producers mean that numerous factors will lion by 2050, and since steps are unlikely to be impinge on any attempt to introduce alternative taken to regulate population growth, the level methods of managing nematodes. The soil environ of innovation that characterized the latter ment; the soil biota; the role of organic matter; part of the 20th century will have to continue the biological interactions that occur at the unabated for many more years. Thus, the root–soil interface; the soil food web; and the challenge facing agriculture is to meet the soil nematode community were discussed in food requirements of a larger and more afflu- Chapters 2 and 3. This chapter aims to cover ent population in an era when food producers some of the agricultural issues that affect our are experiencing greater competition for land, attempts to establish reliable systems of biological water and energy (Godfray et al., 2010; control. Land managers and farmers live in the real Gomiero et al., 2011a). world, and so their management options are Increases in crop production derive from limited by climate, the inherent properties of the three main sources: expansion of arable land; soil resource, economics, market requirements increases in cropping intensity (the frequ and many other factors. Alternative pest control ency with which crops are harvested from a strategies will only be adopted if they are feasible, given area); and improvements in yield. Since cost-effective and consistently successful. the 1960s, the United Nations Food and Agriculture Organization (FAO) has shown that yield improvements made by far the Global Food Security greatest contribution to the increase in global food production, accounting for about 78% of Agriculture is a vibrant, innovative and suc- the increase between 1961 and 1999. The cessful industry. Despite a doubling of the remainder came from an expansion in the global population in the last 50 years, food arable area (15%) and increased cropping

intensity (7%) (Bruinsma, 2003). Future pro- reduce erosion by increasing plant biomass, jections suggest that this situation is unlikely root growth and ground cover; and (vi) the to change. There will be opportunities to cultivation of legumes in cropping and expand the arable area in sub-Saharan mixed crop–livestock farming systems will Africa and Latin America, but in developing add nitrogen to soils and improve their sta- countries overall, 80% of increased crop bility and texture. production will have to come from intensifi- Attention to issues associated with soil cation, higher yields, greater levels of mul- degradation will always be an important pri- tiple cropping and shorter fallow periods. ority for land managers, but the important In developed economies, where agricul- message from the previous paragraph is that tural land is increasingly being planted to as food production becomes more intensive, energy-producing biomass crops, virtually many practices are available to minimize all the required increase in food production soil degradation, and they must be compo- will come from yield improvements and nents of future soil management programmes. intensification. At the same time, future farming systems The need to produce more food on land will have to address the environmental that is already being used for food crops impact of agriculture. Agricultural activities, raises the question of whether land can be particularly those resulting in emissions to air farmed more intensively without increasing and water, can have significant effects long the rate of soil degradation. Agricultural distances from where those activities take land is automatically degraded when nutri- place. Pesticides and nutrients can move into ents are removed in harvested crops, but surface and ground water, while greenhouse further degradation may occur through gases can be emitted to the atmosphere, and water and wind erosion, desertification, so steps must be taken to minimize these salinization and leaching of nutrients. negative impacts. Practices such as integrated Nevertheless, there are a number of reasons pest management; optimization of water, why agricultural intensification will not nutrient and pesticide inputs through pre- necessarily increase the rate of these pro- cision agriculture; and a whole range of cesses: (i) evolving technologies in no-till/ practices to conserve soil and water (e.g. con- conservation agriculture can maintain year- servation tillage, cover cropping, controlled round soil cover and increase soil organic traffic, contour farming and mulching) will matter, thereby reducing water and wind also have to be adopted more widely by erosion while maintaining soil health; farming communities. Food production must (ii) most irrigated agricultural land is rela- continue to increase in the 21st century, but it tively flat and is little affected by erosion, will have to be done in an environmentally while abandonment of marginal land that is sustainable manner, a process that has been too steep for agriculture, together with prac- termed ‘sustainable intensification’ (Royal tices such as contour banking, will reduce Society, 2009). water erosion; (iii) agroforestry (the integration of cropping and or/livestock production with trees or shrubs) offers opportunities to reduce soil erosion, restore soil fertility Sustainable Farming Systems and increase biodiversity; (iv) a shift towards raising livestock in more intensive Responsible and enduring stewardship of systems will reduce grazing pressures on agricultural land is the essence of sustainable dryland pastures; (v) a range of intensifica- agriculture: land is managed in ways that tion practices (increased fertilizer con- maintain its long-term productivity, resilience sumption, more efficient fertilizer use, the and vitality while minimizing adverse environ introduction of drought- and salt-tolerant mental impacts. Although it has been vari- crops, the use of grazing-tolerant pastures ously defined (Hamblin, 1995; Lewandowski and the introduction of irrigation) will et al., 1999; Gliessman, 2007; Gold, 2007; Global Food Security and Sustainable Agriculture 79

Pretty, 2008), sustainable agriculture is (Pretty, 2008). However, a number of key generally considered to: (i) replenish the practices are consistently associated with resource base that sustains agricultural pro- sustainability (Goulding et al., 2008; Shennan, duction, and then maintain it in a condition 2008; Wilkins, 2008; Kassam et al., 2009), and that does not compromise its use by future they are summarized next. Applied together, generations; (ii) integrate biological and or in various combinations, these practices ecological processes such as nutrient work synergistically to increase productivity cycling, nitrogen fixation, soil regeneration, and also to contribute important ecosystem allellopathy, competition and the regula- services that enhance sustainability. How tory effects of pests’ natural enemies, into ever, it is important to recognize that there is food production systems; (iii) utilize eco- no prescriptive list of sustainable practices: logical knowledge, the basics of agricul- farmers have many options available to them, tural science and the management skills and their management practices must be cho- and ingenuity of farmers to develop farm- sen and adapted according to local production ing systems appropriate for the soil, conditions and environmental constraints. climate and production goals; (iv) optimize the use of resources and minimize the Reduced tillage use of non-renewable inputs; and (v) mini- The negative impacts of mechanical tillage mize the impact of pest management, crop on soil carbon reserves and the increased nutrition, irrigation and other produc- susceptibility of cultivated soil to water and tion practices on human health and the wind erosion have demonstrated that farm- environment. ing systems based on inversion tillage are Sustainable agriculture is not a pre- not sustainable. Many options are available scribed set of practices. It challenges land to reduce the depth, frequency and intensity managers to think about the long-term of tillage operations, but no-till is associated implications of the practices they use, and to with the least physical disturbance. It understand the interactions that occur improves levels of soil organic matter, has within and between the many components profound direct and indirect effects on soil of agricultural systems. A key goal is to view structure and aggregation, does not disrupt agriculture from an ecological perspective the soil biota, minimizes the consumption of and balance the requirements for productiv- fossil fuels and reduces labour requirements. ity and profitability with an understanding Since a move to reduced tillage can increase of nutrient and energy dynamics and the compaction problems, particularly in farm- biological interactions that occur in agroeco- ing systems with heavy equipment and ran- systems. Any new practice or technology dom traffic, controlled traffic systems are that improves productivity for farmers but usually an integral component of no-till does not cause undue harm to the soil agriculture. biological environment is likely to enhance sustainability. Continual cropping and maintenance of a permanent cover of plant residues

Sustainable agricultural intensification This component of intensification minimizes the length of fallow periods and helps to Sustainable agricultural intensification is ensure that the resources provided by roots essentially about increasing productivity in ways and their exudates are continually available that make better use of existing resources to the soil biological community. Continual while minimizing environmental harm. cropping (within the limits imposed by the There are many pathways to agricultural environment) and maintenance of a protec- sustainability, and no single configuration of tive cover of organic matter on the soil sur- technologies, inputs and management prac- face mimics, to some extent, the way plants tices is likely to be applicable in all situations and soil interact in the natural environment. 80 Chapter 4

Roots produced by previous crops are not prevent the world’s major food crops from disturbed, while the residues produced by being regularly decimated by rusts, mildews the primary crops and any cover crops are left and a range of insect and nematode pests, and on the soil surface, where they moderate tem- do so in such an effective manner that fungi- perature fluctuations, conserve water and cides, insecticides and nematicides are not nutrients, protect the soil from erosion, mini- widely used on many crops. However, there mize weeds and promote soil biological are concerns that plant breeders working activity. Thus, crop residues are seen as a in high-input systems have inadvertently valuable resource in a sustainable farming selected plants with poor root systems; that system, rather than something that should be higher external inputs are often needed to burnt or removed because it is a hindrance to obtain improved yields; and that genetic uni- future production. The extent of the benefits formity and a narrowing of the genetic base from residue retention will depend on the may lead to decreased resilience in the face of quantity and quality of the residues pro- environmental stress. Future plant-breeding duced, and how they are manipulated. programmes must, therefore, concentrate on producing well-adapted varieties that not Greater plant diversity only resist or tolerate the effects of important pests and pathogens, but also have a root The practice of crop rotation plays a vital role structure and biomass capable of retrieving in sustainable agriculture, as it is one of the nutrients effectively. The cultivars available in simplest ways of minimizing losses from future must also have a greater capacity to pests and pathogens that are often relatively cope with common abiotic stresses such as crop-specific. However, there are many other heat, drought and salinity. options that can be used to increase bio logical diversity within agroecosystems, and Optimized crop nutrition enhance system resilience and sustainability. Examples include the maintenance of natural In many modern farming systems, fertilizers habitats in farming areas; integration of vari- and manures are applied excessively because ous forms of forestry with agriculture; the use the economic response in crop yield far out- of intercrop systems in which multiple crops weighs the cost of the fertilizer. Consequently, are grown in mixed or structured arrange- enormous quantities of fertilizer are being ments; the planting of hedgerows and alley wasted. For example, about 50%, and some- crops or the introduction of banker plants to times even more, of the synthetic nitrogen encourage predators of pests; the retention or applied to crops is usually lost to the environ- provision of windbreaks; and the introduc- ment as gaseous emissions to the atmosphere, tion of legumes to fix nitrogen. In the long leaching to groundwater, and runoff to sur- term, research aimed at replacing annual face waters (Tomich et al., 2011). Improved grain and oilseed crops with perennials (see nutrient-use efficiency must, therefore, be one Cox et al., 2006; Glover et al., 2007) will not of the cornerstones of sustainable intensifica- only provide opportunities to increase crop tion. This is not an impossible task, as many diversity, but also help to make agriculture relatively simple practices are available to more sustainable. optimize crop nutrition. Some of the options include the use of soil analyses to determine Improved crop yield potential nutrient requirements; application of lime to maintain the appropriate pH for optimum The process of improving crops through plant nutrient supply; use of leaf and sap analysis breeding and genetic modification has played to match nutrient applications to the crop’s a major role in increasing world food produc- requirements; inclusion of organic soil amend tion over the last 50 years. However, the ments in the nutrition programme; use of effects on agricultural sustainability have controlled-release fertilizers or nitrogenous been mixed. On the positive side, modern products containing nitrification inhibitors; crop varieties with pest and disease resistance and the introduction of legumes to provide Global Food Security and Sustainable Agriculture 81

biologically fixed nitrogen. Ultimately, how- disease occurrence, crop growth, harvestable ever, sustainable nutrient management must yield) offers the potential to improve sustain- also take into account the nutrients immobi- ability by maintaining or enhancing crop lized and mineralized by the soil biota. Inter yields while reducing some of the environ- actions between soil organisms and organic mental problems associated with nutrient matter govern nutrient availability to plants, and pest management. and greater efforts must be made at a research level to reliably predict the outcome of these Integrated pest management interactions, so that nutrient applications can be adjusted accordingly. Integrated pest management has been defined in various ways (Stirling, 1999), but is essentially about using our knowledge of pest and Efficient water management plant biology to prevent pests from causing Although only about 18% of the world’s economic damage. Pest populations are moni- cropped land is irrigated, this land is vitally tored; damage thresholds are determined; the important, as it produces about 45% of the impact of environmental factors on interactions global food supply (Morison et al., 2008). between the pest and the plant are understood; However, irrigation water will always be a a wide range of techniques (e.g. genetically scarce resource due to the competing dem resistant hosts, environmental modifications ands of agriculture and industry, and the and biological control agents) are used to requirements for human consumption. From reduce pest populations to tolerable levels; an agricultural perspective, misuse of irriga- and pesticides are only used as a last resort. tion water results in soil health and environ- IPM systems that reflect this philosophy will mental problems, while current and future enhance sustainability because they are based water supplies will be depleted if irrigation on sound ecological principles. use outpaces recharge rates. Thus, efficient water management is the key to sustainable Integrated crop and livestock production irrigated agriculture. It can be achieved by improving irrigation infrastructure; by reducing One factor that impacts negatively on the sus- evaporative losses; and by matching water tainability of modern agriculture, particularly inputs to the crop’s requirements through in developed countries, is the trend towards the use of technologies that monitor soil farm-level specialization. Crop production is moisture, environmental conditions and becoming more specialized and crop and live plant growth. stock enterprises are often separated, despite the clear soil health and environmental benefits associated with mixed crop–livestock sys- Site-specific management tems. Farm livestock excrete some 50–95% Precision farming or site-specific manage- of the nutrients they consume, and from an ment involves observing, measuring and efficiency and sustainability perspective, there then responding to intra-field variability so is a strong case for better integration of crop that agronomic practices and resource alloca- and livestock production, both at the individ- tion are matched to soil and crop require- ual farm and regional level (Wilkins, 2008; ments. Nutrients, pesticides and other inputs Kirkegaard et al., 2010). are applied differentially using predefined maps based on soil or crop condition, or with sensors that control application as machinery Soil Health traverses the field (Srinivasan, 2006). The capacity of precision agriculture to vary The quality or health of the soils used to pro- inputs based on variability in soil properties duce crops and livestock is intimately linked (e.g. soil texture, water-holding capacity, to the issue of sustainable agriculture. Although organic matter status), or biological factors some minor crops are grown hydroponically – (e.g. weed populations, insect populations, and commercial facilities may be established 82 Chapter 4

to produce livestock, poultry and fish – food attribute believed to be reflective of ‘natural’ production is largely dependent on the thin benchmark conditions, and those who argue layer of soil that covers the earth’s surface. that production agriculture is not a natural This non-renewable resource has a number of system, and that the debate should be about ecologically important functions: providing how soils are managed to achieve the required a suitable medium for plant growth; sustain- production and environmental outcomes. ing biological processes responsible for decom The terms ‘soil health’ and ‘soil quality’ are posing organic matter; cycling nutrients; often used synonymously, but the former term maintaining soil structure; regulating pest is used here because most farmers have at least populations; and detoxifying hazardous com- some understanding of the concept. Soil is pounds (Powlson et al., 2011a). It is important healthy if it is fit for a purpose, which in the case from an agricultural production, environ- of agriculture is the production of a particular mental and sustainability perspective that crop. However, agricultural land is a component those functions are maintained indefinitely. of a larger ecosystem, so it must also provide Although it is widely recognized that functions that prevent degradation of neigh- maintaining healthy soil is a vital component bouring environments. The definition used by of sustainable agriculture (Doran et al., 1994; Kibblewhite et al. (2008) encompasses both of 1996; Lal and Stewart, 1995; Doran and Safley, these important functions: 1997; Rapport et al., 1997; Gregorich and a healthy agricultural soil is one that is capable Carter, 1997; Kibblewhite et al., 2008), the term of supporting the production of food and ‘soil health’ has been the subject of fierce fibre, to a level and with a quality that is debate in the scientific literature (Sojka and sufficient to meet human requirements, Upchurch, 1999; Karlen et al., 2001; 2003a,b; together with continued delivery of other Letey et al., 2003; Sojka et al., 2003). First, argu- ecosystem services that are essential for ments abound as to how soil health should be maintenance of the quality of life for humans defined and whether ‘soil quality’ is a more and the conservation of biodiversity. appropriate term. Second, it has been particularly difficult to find a definition of soil quality/soil health that satisfies everyone, because Management impacts on soil health and soil performs multiple functions simultane- the role of conservation agriculture ously. Thus, high soil quality for one function (e.g. crop production) does not guarantee Farmers and land managers are well aware of high quality for another function (e.g. envir the many constraints that affect the produc- onmental protection), and vice versa. Third, tivity of the soils used for agriculture. Those attempts to develop soil-quality indices have constraints are too numerous to discuss here, been criticized on the basis that the process but include soil compaction; poor structure; does nothing more than provide a highly surface crusting; limited water infiltration; generalized and non-specific assessment of excessive leaching of nutrients; susceptibility the overall worth, value or condition of a soil. to erosion; high weed pressure; poor nutrient One of the major concerns is that assess- retention; low water-holding capacity; nutri- ment tools do not objectively and simultane- ent deficiencies; sub-optimal pH; excessive ously consider both the potential positive salinity; low biological activity; limited bio- and negative impacts of all indicators on pro- logical diversity; and high levels of soilborne duction, sustainability and the environment. pathogens. Although most soils have only Thus, some highly valued parameters such as some of these problems, no soil could ever levels of soil organic matter and numbers of be considered completely healthy from a pro- earthworms are almost always viewed posi- duction perspective, while environmental tively, even though an increase in these issues such as off-site movement of nutrients parameters may sometimes result in negative and pesticides, and greenhouse gas emissions, outcomes. Finally, there are differences between are universal problems. Thus, one of the those who evaluate soil health or quality on the most important roles of a farm manager is basis of biodiversity, bioactivity or some other to identify and prioritize the main factors Global Food Security and Sustainable Agriculture 83

causing soil-related problems, and then nitrogen due to immobilization; exacerbation attempt to improve the health of the soil of diseases caused by pathogens that survive through management. on crop residues; difficulties associated with In a complex system such as soil where managing some weeds in the absence of till- many factors interact, the most robust ap age; herbicide carryover and runoff; the proach to soil health problems is to consider potential for weed populations to become how a farming system could be modified to resistant to herbicides; and the impact of soil rectify existing problems and prevent them organic matter and earthworm burrowing on from recurring. For example, poor soil health porosity and macropore formation, which can is often associated with low levels of soil increase the risk of nutrients and pesticides organic matter, and so tackling that issue in becoming groundwater contaminants. particular can lead to improvements in a whole The individual economic, soil health range of soil physical, chemical and biological and other benefits listed in Table 4.1 will not properties. Thus, the practices previously be obtained in every situation, but collec- identified as the keys to sustainable agricul- tively these benefits provide compelling rea- ture are also the keys to improving soil health. sons for farmers to minimize tillage and The three most important soil improve- incorporate residue retention and crop rota- ment practices (minimal soil disturbance, tion into their farming systems. However, permanent plant residue cover and crop rota- perhaps the most persuasive reason for tion) form the basis of conservation agricul- adopting the soil and crop management prac- ture (Baker et al., 2006; Hobbs et al., 2008; tices associated with conservation agriculture Kassam et al., 2009), a relatively recent agri- is that they enhance soil organic carbon pools, cultural management system that has been thereby reducing atmospheric CO2 emissions adopted widely in some parts of the world, associated with climate change (Powlson particularly North America, Latin America et al., 2011b). Continuous surface cover and and Australia. Conservation tillage (variously the increase in water-holding capacity associ- described as minimum tillage, reduced till- ated with higher levels of soil organic matter age, no-till or direct drill) and retention of crop also help mitigate the effects of any change in residues are the primary components of con- climate by increasing the tolerance of crops to servation agriculture, and when used together, higher temperatures and drought conditions these practices reduce soil erosion and slow (Lal, 2009: Lal et al., 2011). or reverse the precipitous decline in soil organic matter that has occurred in conven- tionally tilled agricultural soils over the last Other management practices 100 years (Reeves, 1997; Uri, 1999; Paustian to improve soil health et al., 2000; Franzluebbers, 2004). When com- bined with diversified crop rotations that Although integrating conservation tillage, include cover crops, mulch-producing crops residue retention and crop rotation is the first and nitrogen-fixing legumes, many soil prop- step towards greater sustainability and erties are affected (Table 4.1), soil health improved soil health, further incremental generally improves, and suppressiveness to improvements can be obtained by adopting a root pathogens is often enhanced (Sturz et al., range of other practices. 1997). However, as pointed out by many authors, including Blevins and Frye (1993) Well-adapted, high-yielding varieties and Sojka et al. (2003), there are situations where the effects of conservation agriculture Genome sequencing, DNA marker technolo- and increased levels of soil organic matter are gies, and phenotype analysis are just some not always positive. Examples include the imp of the many tools currently being used by act of mulch cover on soil temperature, which plant breeders to improve the resistance of can improve crop growth in a hot climate but crops to pests and diseases, and to increase slow early emergence and growth in temperate their tolerance to abiotic stresses. The addi- regions; decreased availability of plant-available tional biomass produced by higher-yielding 84 Chapter 4

Table 4.1. The effects of the principal components of conservation agriculture on soil health and sustainability.

Component

Mulch cover No tillage Crop rotation (crop residues, (minimal or (includes legumes cover crops, no soil for nitrogen Effect green manures) disturbance) fixation)

Maintains a permanent residue cover on the soil surface + + + Reduces evaporative loss from upper soil layers + + Maintains the natural stratification of the soil profile + + Minimizes oxidation of soil organic matter +

Sequesters carbon and minimizes CO2 loss + + + Minimizes compaction by intense rainfall + Minimizes temperature fluctuations at the soil surface + Maintains a supply of organic matter for the soil biota + + + Increases and maintains nitrogen levels in the root zone + + + Increases cation exchange capacity + + + Maximizes rainfall infiltration and minimizes runoff + + Minimizes erosion losses from water and wind + + Increases water-holding capacity + + Minimizes weeds + + Increases the rate of biomass production + + + Speeds the recuperation in soil porosity by the soil biota + + + Rebuilds damaged soil conditions and dynamics + + + Recycles nutrients + + + Reduces pests and diseases + Reduces labour input + Reduces fuel-energy input +

Modified from Kassam et al. (2009). crops should result in soil organic matter Efficient water management gains that will improve the health of agricultural soils. Well-adapted, disease-resistant The soil health and environmental problems varieties could also help to reduce the off-site associated with irrigation are widely recog- impacts of agriculture, provided they have nized. Water tables rise when irrigation water root systems that utilize applied nutrients more is applied; salinity is a constant threat to irri- effectively than their susceptible counterparts. gated agriculture; excessive inputs of water cause waterlogging and drainage problems; Optimal nutrient management and salts, nutrients, herbicides and pesticides that are leached through the soil pro- In soils used for agriculture, nutrient levels file or transported by overland water flow must be maintained by replacing the nutri- will reduce the quality of downstream water. ents removed in the harvested product. However, it is possible to avoid these nega- However, whenever industrially produced tive impacts. Trickle irrigation; precision land fertilizers and their organic alternatives are levelling to improve surface irrigation; and applied excessively, the nutrients they con- monitoring soil water at multiple depths in tain will either become environmental pol- the profile and then using the data to match lutants or be detrimental to some components irrigation inputs to plant uptake are just some of the soil biota. Thus, high nutrient-use effi- of the practices that will markedly reduce ciency is an important component of main- deep percolation losses to groundwater. taining soil fertility, but is also essential for Deficit irrigation and partial root-zone drying minimizing off-site impacts. are other management techniques that can be Global Food Security and Sustainable Agriculture 85

used to improve water use efficiency and detect weeds and ensure that chemical or minimize the off-site impacts of irrigation non-chemical weed controls are applied (Loveys et al., 2004; Morison et al., 2008). only where they are needed. Thus, variable- rate application minimizes the environmen- Integrated pest management tal footprint of farming, reduces costs and ensures that soil is not degraded by exces- Although IPM is widely promoted as a pest sive external inputs. and disease-control strategy, the rates of A range of soil sensors is available in pre- adoption and the tactics employed vary cision agriculture to measure various soil considerably from industry to industry and physical and chemical properties (Adamchuck from one pest to another. In some crops, et al., 2004), while geo-referenced soil sam- pest populations are monitored and crop ples are widely used to determine nutrient losses are minimized by integrating various requirements in fields that may vary in soil cultural and biological controls, while in type, topography, cropping history or previ- others, IPM involves little more than pesti- ous fertilizer inputs. Such samples can also cide management. In situations where be used to obtain an accurate base map of insecticides and fungicides are included in organic matter status. Although such infor- IPM programmes for above-ground pests, mation is a useful starting point for manag the possibility that residues could impact ing the soil biological community in a negatively on the soil biological community site-specific manner, the ultimate research is rarely considered. Thus, the ultimate objective should be to provide growers with land management objective should be to data on the spatial and temporal variability develop a fully integrated system of man- of key soilborne pests and their natural en aging the soil, the crops, and all pests and emies. High-throughput molecular methods diseases. The IPM component would ide- of enumerating soil organisms are currently ally be effective enough to control the key too expensive to be used in diagnostic services, pests with minimal need for pesticides, but since this will change with improve- while the crop and soil management comments in sequencing methods and advances ponent would aim to generate a healthy, in bioinformatics, it will eventually be pos biologically active soil capable of degrad- sible to integrate molecular diagnostics ing any pesticide that might be required, with the technologies available in precision thereby preventing it from becoming an agriculture. environmental contaminant. Integrated crop and livestock production Variable-rate application and site-specific management The permanent nature of pastures and the continual presence of perennial plant species Intra- and inter-field variability in soil prop- mean that soils under pasture are generally erties such as texture, depth, nutrient con- healthier than cropped soils. Pasture-based crop tent and disease levels are the norm in an and livestock production systems (e.g. mixed agricultural landscape. Variable-rate appli- farming systems and zero-grazing cut-and-carry cation techniques associated with precision systems) also require fewer external nutrient agriculture provide the tools to optimize inputs than systems dominated by crop- management in such situations. Soil varia- ping, and so they tend to be more sustainable bility across a field is mapped, a satellite (Wilkins, 2008). Also, in landscapes that are positioning system (e.g. GPS) determines subject to dryland salinity, the inclusion of the location of farm equipment within the deep-rooted perennials such as lucerne in a field, and variable-rate applicators can then cropping rotation reduces deep drainage and apply fertilizers, pesticides and biological prevents salinization (Bellotti, 2001). Thus, products in amounts that are appropriate from soil health and sustainability perspec- for the crop’s needs in a given location. In tives, it makes sense to integrate livestock the same way, optical sensors are used to production and cropping. 86 Chapter 4

Ecologically sound management systems: In Australia, grain is grown in a wide the pathway to healthy soils variety of climatic zones (dry subtropics to cool temperate and Mediterranean climates) The ultimate challenge of agricultural land and on vastly differing soil types (from heavy management is to integrate the best available clays to coarse sands), and crops are almost practices into a farming system that is not always produced under rainfed conditions. only productive and profitable, but also Rainfall is generally low and highly variable, sustains the soil’s productive capacity. The with most cropping regions receiving actual farming system that is chosen will between 250 and 600 mm of rain per year. depend on climatic factors, the basic proper- However, despite the limitations of soil and ties of the soil being farmed, the resources climate and the absence of government subsi- available to implement change, and the com- dies, Australian agriculture has achieved modity being produced. However, there is greater productivity growth than most other little doubt that major improvements are agricultural economies over the last 30 years possible in all the world’s current farming (Mullen, 2007). This success has largely been systems. The fact that the principles of con- achieved through the widespread adoption of servation agriculture are being incorporated conservation agriculture. Although manage- into a diverse range of farming systems in ment practices vary at a regional and local developed and developing countries around level, most leading farmers have made the the world (Hobbs et al., 2008; Kassam et al., change to no-till agriculture; crops are sown 2009) is testimony to the fact that progress is using equipment that incorporates improved being made. disc-seeding technologies; in-field traffic is controlled using GPS guidance; rotational cropping or pasture leys are included in the farming system; legume crops provide nitrogen Soil-health benefits from conservation inputs; crop residues are retained on the soil agriculture and precision farming: surface; scanning technologies and variable- Australian examples rate injection systems are used to optimize chemical application; optical-sensing devices Conservation agriculture is widely practised ensure that herbicides are applied on weeds in five countries: the United States, Brazil, rather than on bare soil; while in-vehicle, Argentina, Canada and Australia, but the aerial or remote sensing systems are available Australian situation is of particular interest. to provide information on environmental fac- Australia has the poorest soils and one of the tors such as temperature and humidity, and most variable climates in the world, and its the health status of the crop. successes with conservation agriculture sug- From the perspective of soil health, the gest that the principles involved could be introduction of these practices has gener- adopted by farmers producing almost any ally had a positive effect. The move towards crop, in most regions of the world. Australia’s reduced-till and direct-drill systems, with major crops are grains (wheat and other cer associated stubble retention and traffic con- eals, pulses and oilseeds) and sugarcane, and trol, has improved most measures of physical the practices now used to produce those structure (e.g. aggregate stability, the pres- crops, and their impact on productivity and ence of stable macropores and shear strength) soil health, are summarized next. Further and also reduced compaction, thereby revers- detail on grain-cropping systems can be ing the negative effects of conventional tillage obtained from various chapters in Tow et al. on soil physical properties. Soil organic car- (2011); the sugarcane farming system is dis- bon levels have generally improved, particu- cussed by Garside et al. (2005); while issues larly in the upper 10 cm of the profile, associated with soil health and the soil biota although studies in some environments have are reviewed by Bell et al. (2007), Stirling shown no significant change. The develop- (2008), Gupta and Knox (2010) and Gupta ment of biologically mediated suppression of et al. (2011). two of the most important soilborne diseases Global Food Security and Sustainable Agriculture 87

of wheat (Rhizoctonia bare patch and take- then replant the field to sugarcane. A multi- all) has also been observed in long-term disciplinary research team was established to experiments and some commercial fields develop solutions to the problem, and its ini- (Roget, 1995; Roget et al., 1999; Pankhurst tial studies showed that soils under long-term et al., 2002; Gupta et al., 2011) and is associated sugarcane monoculture were physically and with a build-up of organic carbon and micro- chemically degraded. Results of later experi- bial biomass under direct-drilling with stub- ments indicated that biological constraints ble retention (Pankhurst et al., 2002). There is were also limiting productivity, as large yield also evidence that soil in the upper 25 cm of responses were obtained when soil fumi- the soil profile is suppressive to root lesion gants, fungicides and nematicides were nematode, Pratylenchus thornei, a major con- applied; or pasture, another crop species, or straint to production in subtropical grain- bare fallow were included in the rotation growing areas (Stirling, 2011b). Another (Garside and Bell, 2011a, b). Ultimately, the important soil-health benefit has been an 12-year research programme (summarized by increase in the capacity of soils to infiltrate Garside et al., 2005; Stirling, 2008) resulted in and store water, and an improvement in the the development of a new farming system ability of roots to extract water from the soil based on permanent raised beds, residue (Turner, 2004). Therefore, crops are much retention, minimum tillage, a leguminous more likely to reach their water-limited yield rotation crop and controlled traffic using potential, with concomitant effects on pro- GPS guidance. This system is now being ductivity and the amount of organic matter adopted by growers because it increases returned to soil. Because there have also been sugar yields, reduces costs and provides negative effects in some situations (e.g. slower additional income from rotation crops such early-season growth under direct drill, nutri- as soybean and peanut. ent stratification in surface soils and increases Although economic considerations (lower in diseases such as crown rot where patho- fuel and labour costs, and the replacement of gen inoculum survives on stubble), ongoing fertilizer nitrogen with biologically fixed research and constant fine-tuning by farmers nitrogen from legumes) motivated growers to is required to continually improve and fully adopt the new sugarcane farming system, optimize the new system. improvements in soil health were the main The Australian sugar industry is vastly reason that yield increases of 20–30% were different from the grains industry. Farms are consistently obtained. Random trafficking of much smaller (commonly 40–200 ha), the fields, often in wet conditions, by the heavy crop is grown largely as a monoculture, and machinery used to plant, harvest and trans- inputs of fertilizer and pesticides are much port the crop meant that soil compaction higher. Also, the industry’s location in the was a major problem in the previous farm- tropics and subtropics means that water is not ing system. Soil physical properties improved a limitation: between 1200 and 4200 mm of markedly when beds were widened to accom- rain is received each year, and in the drier modate controlled traffic. The introduction of areas, rainfall is supplemented by irrigation. a rotation crop reduced populations of fun In the early 1990s, the Australian sugar gal and nematode pathogens that were con- industry was facing an uncertain future straining crop production. A reduction in till- because productivity was declining due to a age increased earthworm populations, with problem known as yield decline. At that time, consequential effects on macroporosity and sugarcane was grown on beds 1.5 m apart, water infiltration rates. In rainfed situations, machinery wheel spacing did not match crop improved water capture in periods of low row spacing, and the crop residues remaining rainfall contributed to yield increases, while after harvest were often burnt. After a plant improved percolation through macropores and 3–4 ratoon crops, an expensive pro- and retention of surface cover protected soils gramme of ripping and cultivation was from erosion during intense tropical storms. required to remove the old crop, alleviate There have also been signs of improvement in compaction caused by farm machinery and some chemical, biochemical and biological 88 Chapter 4

properties associated with soil health (Stirling by numerous physical, chemical and bio- et al., 2010), and surface soils are now sup- logical properties, and the way they interact. pressive to Pratylenchus zeae, the main However, the literature is replete with lists nematode pest of sugarcane (see Chapter 11 of measurable properties that collectively for details). Further improvements are expec provide a broad indication of the health of ted to occur over time, but it is likely to a soil, and can be used to assess the impact take at least 15 years to fully realize the ben- of soil management practices on soil health efits from the new farming system (Stirling (e.g. Doran and Parkin, 1994; Pankhurst et al., 2010, 2011b). et al., 1997). A variety of physical, chemical In summary, these Australian examples and biological parameters are usually show that: (i) the principles of conservation measured during the soil-health assess- agriculture are applicable in diverse envir ment process (e.g. Idowu et al., 2009) and a onments and quite different farming sys- subset of these indicators is then used to tems; (ii) major changes in farming systems compile a relatively simple report that is can be made relatively quickly in an envir designed to help growers make manage- onment where there is a strong level of ment decisions (e.g. Gugino et al., 2009). agronomic research and good communica- Although such reports are useful, the prac- tion between scientists, extension personnel ticality of measuring numerous parameters and farmers; and (iii) the economic and is often questioned, as certain parameters other benefits of conservation agriculture (e.g. total carbon and labile carbon) are (e.g. reduced labour costs, much lower often closely correlated with the physical energy inputs, improved timeliness of oper- and chemical properties assessed in soil- ations and greater profitability) are so com- health tests. pelling that growers are generally willing to Although it is recognized that most soil consider making changes to their farming properties are ultimately determined by system. interactions between soil organic matter Although minimum tillage, residue and the soil biota, biological measurements retention and crop rotation interact together are rarely included in soil-health tests, as to improve a whole range of physical, chem levels of organic matter and active carbon ical and biological properties associated with are often used as surrogates for biological soil health, this does not mean that farming activity and diversity. Hundreds of ‘poten- systems based on these practices are problem- tially useful’ biological indicators have free. Numerous issues are the subject of con- been proposed, but in many cases they sim- tinuing research (e.g. nutrient stratification; ply reflect the discipline bias of the propo- management of herbicide-resistant weeds; nent. Also, most do not meet the criteria overcoming soil structural problems during proposed by Doran and Zeiss (2000) as the transition to minimum till; alternative being required for any biological parameter crops for inclusion in rotations), while grow- that is to be used as an indicator of soil ers may need to modify some management health: (i) sensitivity to variations in man- practices to fit the soil and climatic conditions agement; (ii) well-correlated with beneficial on their farms. It is also recognized that soil soil functions; (iii) useful for elucidating organisms are a major determinant of a soil’s ecosystem processes; (iv) comprehensible productive capacity, and that further research and useful to land managers; and (v) easy is needed to fully harness the biological and inexpensive to measure. This prompted potential of soil. Ritz et al. (2009) to look for biological indicators that not only provided information on important soil functions, but were also suit- Indicators of soil health able for use in national-scale soil-monitoring programmes. A list of top-ranked indica- Soil health cannot be measured directly, tors was developed (Box 4.1), but at the because a soil’s capacity to produce crops and end of the process, the authors recognized also safeguard the environment is determined that many of the selected indicators did not Global Food Security and Sustainable Agriculture 89

Box 4.1. Biological indicators for use in monitoring soil health or quality

Ritz et al. (2009) ranked the plethora of biological methods that have been suggested for monitoring soil quality and produced a list of 21 biological indicators that were considered ecologically relevant. However, four of these could not be deployed in national-scale monitoring schemes, as further methodological development was required. The remaining indicators have been consolidated into eight groups, and the authors’ comments on each of these groups are outlined as follows.

Soil microbial taxa and community structure using molecular techniques Recent advances in molecular technologies have provided a range of methods that can be used to monitor various components of the soil biological community. Although terminal restriction length polymorphism (TRFLP) analysis has been used widely, the advent of faster, cheaper and higher- resolution sequencing technologies is providing many other options. Molecular methods are useful because high throughput is possible; information on biodiversity is obtained; results can be related to function; and DNA can be archived. However, further work is required to identify the most suitable primers, and to optimize the polymerase chain reaction (PCR), restriction and fingerprinting steps for particular groups of organisms. Also, these methods are extremely sensitive and discriminatory, and so it is not yet known how they are best applied in field situations, where spatial and temporal variability is the norm.

Soil microbial community structure and biomass from phospholipid fatty acids Extracted lipids, in particular phospholipid fatty acids (PLFA), can be used as signature lipid biomarkers in studies of soil microbial communities. The total PLFA content is indicative of total viable biomass. Individual PLFAs (or suites thereof) can be related to community structure, as they are found predom inantly, but not exclusively, in distinct microbial groups (e.g. fungi, bacteria, Gram-negative bacteria and actinobacteria). The main advantage of PLFA profiling is that it is semi-quantitative, does not rely on cultivability and provides wide coverage of the soil microbial community.

Soil respiration and carbon cycling from multiple substrate-induced respiration

Carbon cycling is fundamental to soil function, and the respiration of CO2 from soils, arising from community- level biotic activity, is an intrinsic indicator of carbon cycling. Since measurement of this property in isolation does not provide discrimination, a multiple substrate-induced respiration (MSIR) approach is more useful, as it characterizes how a soil community responds when exposed to a range of carbon substrates of differing chemical status. As it is a laborious process to generate MSIR profiles, this method is constrained by difficulties involved in achieving high-throughput systems.

Biochemical processes from multi-enzyme profiling Biochemical reactions in soils are mediated by enzymes produced by the soil biota. A plethora of individual enzymes can be profiled, relating to virtually any defined biochemical transformation. However, a multiple enzyme fluorometric approach is particularly useful, as sensitive measurements can be made on small samples; high-throughput assay systems are possible; and several ecological processes can be assessed in a single assay. Another advantage of this approach is that many different fluorescently labelled substrates are available to target carbon-transforming enzymes, and phosphatase and sulfatase activity.

Nematodes The potential of nematodes as biological indicators has long been recognized, as they are abundant in soil and have a wide range of feeding habits. The total number of nematode taxa, the abundance of individual functional groups and a wide range of indices that reflect the composition of the nematode community are widely used as indicators. Since nematode extraction methods are laborious, and highly trained experts are required to identify nematodes (even to functional group level), ultimately nematode community analysis will be carried out using molecular techniques.

Continued 90 Chapter 4

Box 4.1. Continued.

Microarthropods Acari (mites) and Collembola (springtails) have been proposed as potential biological indicators because they are the dominant arthropods in many soils. Extraction methods are fairly straightforward, but the use of arthropods as indicators has been limited by the need for expert skills in identification, and by concerns about which metrics are most useful in ecological studies.

On-site visual recording of soil fauna and flora Organisms that are readily visible (ants, earthworms and fungal fruiting bodies) are considered useful biological indicators because data can be collected relatively easily. However, consistent methodologies are required before such parameters can be used in on-site recording.

Pitfall traps for ground-dwelling and soil invertebrates Pitfall traps are a well-established technique for assessing ground-dwelling and soil invertebrates, and are used widely in environmental surveillance. However, one disadvantage is that return visits are required to collect data.

satisfy all of the criteria considered essential to quantify populations of nematode or insect by Doran and Zeiss (2000). Also, they did not pests; measure the inoculum density of par- know whether the indicators would prove to ticular pathogens; or assess the suppressive- be reliable when used across diverse land- ness of the soil to key pests or pathogens. The scapes, and under environmental conditions latter characteristic is a particularly useful that vary from season to season. indicator of soil health, because a capacity to Soil microbial biomass is one of the sim- prevent soilborne pests from multiplying to plest and most widely used means of estimat- destructive levels demonstrates that an active ing a soil’s biological status, but it did not and diverse biological community is present, appear in the suite of top-ranked indicators and that the regulatory functions within identified by Ritz et al. (2009), largely because it the soil food web are operating effectively. was seen as a relatively gross measure that did Unfortunately, however, there is not yet not discriminate between various components any simple way to assess suppressiveness to of the soil biological community. Gonzales- root diseases. Pathogen-specific bioassays are Quiñones et al. (2011) generally agreed with time-consuming and labour-intensive; multi- that assessment, and argued that soil biomass ple measurements are required to monitor data would be more useful if critical values characteristics that are related to suppressive- were established at a regional level for specific ness (e.g. resilience in the face of a disturbance soil type × land use combinations. They also or stress event); and the various microbial indicated that the relationship between soil parameters that have been assessed do not microbial biomass measurements and manage- show consistent relationships to suppressive- ment practice would have to be better under- ness (van Bruggen and Semenov, 2000; Janvier stood before farmers could use this parameter et al., 2007). as a reliable indicator of soil health. Although a paucity of reliable biological indicators limits the value of most soil-health assessments, an even greater problem is that Ecological Knowledge, Biotic soilborne pests and pathogens are usually Interactions and Agricultural ignored. A soil cannot be considered healthy Management if the crops that are grown in it suffer losses from soilborne diseases, and yet few of the Modern agriculture faces the twin challenges of data sets used to evaluate soil health attempt being both highly productive and sustainable, Global Food Security and Sustainable Agriculture 91

and as Gliessman (2007) pointed out, this the limitations of soil and climate. Since there can only be achieved by applying ecological is a close association between soil organic concepts and principles to the design and matter and the soil biota, this conceptual frame management of agroecosystems. Although work was extended by Gonzales-Quiñones there is general agreement on the need for et al. (2011) and used to explain the size of an ecological approach to farming, discus- the soil microbial biomass pool. Potential sion on what constitutes ecologically sound soil microbial biomass was considered to be agriculture is often polarized by arguments the maximum microbial population that about what type of farming system (e.g. tra- could be sustained given otherwise non- ditional, organic, biodynamic, conventional, limiting conditions, and was constrained by integrated, community-based, free-range, inherent site and soil characteristics (Fig. 4.1). low input, etc.) is best able to provide the For any particular land-use system, the world’s food needs with the least environ- attainable target value for soil microbial bio- mental impact (Trewavas, 2001, 2004; mass was defined by factors controlling Badgley et al., 2007; Badgley and Perfecto, inputs of organic carbon to soil. Any man- 2007; Cassman, 2007). However, when farm- agement practice that increased carbon ing systems are viewed from an ecological inputs (e.g. greater net primary production perspective, they all contain both positive due to fertilization or irrigation) would and negative elements. Thus, it is more tend to increase attainable soil microbial bio- enlightening to focus on the impact of man- mass towards the potential. For soil-monitoring agement on the ecosystem services provided purposes, two lower limits were added. by the soil biota: production of food and Critical was the soil microbial biomass fibre; maintenance of soil structure; storage value below which biological soil function and supply of nutrients; retention and was lost irreversibly, while constraining release of water; and regulation of popula- described the situation where soil biologic tions of soil organisms. al function still occurred but was at the lower limit of the desirable range of values (Fig. 4.1). Once appropriate attainable values were determined, management action Management effects on the soil biota and could be initiated to move the actual value the limiting role of the environment towards the desired target. Although these concepts are relevant It should be clear from this and preceding to soil carbon and microbial biomass, there chapters that the provision of ecosystem ser- is no reason why they could not be applied vices by the soil biota is intimately linked to to other soil biological characteristics of the quantity and quality of soil organic mat- interest (e.g. the level of nutrient cycling; ter. Management practices determine carbon the extent of biodiversity; the rate of a par- inputs and losses, with flow-on effects to the ticular biochemical transformation; or the soil biota, but levels of soil organic matter will level of suppressiveness to a particular pest also be influenced by climatic factors (par- or pathogen). The advantage of visualizing ticularly temperature and precipitation) and soil biological attributes in this way is that it numerous soil properties (e.g. texture, depth encourages scientists and land managers to and mineral composition). Thus, management consider the edaphic and climatic con- plays an important role in determining the straints that limit what is possible in a spe- biological status of a soil, but the environment cific situation, and then think about how limits what is achievable. management might move levels of a par- The role of environmental factors in ticular attribute from current or actual levels limiting carbon sequestration in soils was towards an attainable target. The challenge recognized by Ingram and Fernandes for biological scientists is to provide farmers (2001), who used the term ‘attainable’ to with some indication of what targets are describe the amount of carbon that could be achievable in a given soil type, land use and sequestered in a particular situation, given environment. 92 Chapter 4

Fig. 4.1. Conceptual diagram showing the size of the soil microbial biomass pool in relation to target values and their defining factors. (From Gonzales-Quiñones et al., 2011, with permission.)

Provision of ecosystem services by the soil the harvested product; (ii) reducing leaching biota and the role of management losses by increasing the soil’s cation exchange capacity; (iii) minimizing denitri- The soil biological community is responsible fication losses through better drainage; for providing a range of ecosystem services, (iv) including legumes in the rotation to and when these natural services are lost supply biologically fixed nitrogen; (v) opti- due to biological simplification, they must mizing mycorrhizal symbioses with plant be replaced by external inputs (Altieri, roots to enhance phosphorus and micro 1999; Shennan, 2008). Thus, insecticides, nutrient uptake; (vi) understanding the nematicides and fungicides are required mineralization and immobilization pro- when regulatory processes are no longer cesses associated with soil organic matter, effective enough to suppress pests and and then adjusting residue management pathogens. The essence of ecologically practices so that naturally cycled nutrients sound agriculture is to understand the bio- are available when they are required by the logical interactions involved in the provi- crop; (vii) ensuring that nutrients are not sion of a desired service and then use that applied in excess of crop requirements; and knowledge to manipulate the biota through (viii) applying nutrients in forms that do management, thereby minimizing or elimi- not impact negatively on key components of nating the need for external inputs. In the the soil biota. case of crop nutrition, this process might Given the number of issues listed above, involve: (i) knowing the level of nutrients it should be apparent that taking an ecological required to replace the nutrients removed in approach to nutrient management is a huge Global Food Security and Sustainable Agriculture 93

challenge. Biotic interactions are important the wider biological community. However, mediators of nutrient availability, but we we are not yet able to define the type of are not yet able to connect population and biological community and the level of community ecology with fluxes of nutrients. biological activity required to maintain Also, the interactions involved in biologic populations of specific pests and patho- al nutrient cycling are complex and often gens at levels that do not cause economic multitrophic, and our understanding of the damage. processes involved is too rudimentary to be used successfully in crop management (Plenchette et al., 2005; Goulding et al., 2008). Results from organic farming systems, Integrated Soil Biology Management where nutrient-cycling processes form the basis of crop nutrition, are testimony to the The material presented in this chapter outlines difficulties involved in taking such an the many issues that must be considered approach to maintaining soil fertility: yields by anyone wishing to manage soil biotic are generally lower than in conventional interactions in such a way that crop produc- farming systems (Posner et al., 2008); the tivity is maintained or improved; soil health biological community is not always enhan is enhanced; off-site environmental impacts ced by organic inputs (Shannon et al., 2002); are minimized; natural processes are contrib- and high levels of mycorrhizal colonization uting to crop nutrition; and regulatory mech- do not necessarily overcome phosphorus anisms are providing some pest and disease deficiency (Kirchmann and Ryan, 2004). control. Clearly, this is an overwhelming task Thus, there is a need for research to better that involves what was referred to in Chapter understand and manage the microbially 1 as ‘integrated soil biology management’: a mediated processes that impact on soil nut management approach that not only requires rient dynamics. A return to more diverse crop-specific and site-specific knowledge, crop rotations and increased use of cover or but a capacity to integrate various practices catch crops, for example, is likely to improve into a productive and sustainable farming soil health and provide some pest and dis- system that provides a full range of ecosystem ease control, but may have both positive services. Although the complexities associ- and negative effects from a nutritional per- ated with this approach are obvious, it is only spective. Fertilizer nitrogen requirements by considering the full gamut of issues that may be reduced and nutrient-use efficiency affect crop production (crops, soils, climate, may improve, but more nitrates may be water, organic matter, crop rotations, tillage leached from the profile, an outcome which practice, nutrients, weeds, pests, diseases indicates that changes in practice do not and beneficial organisms) that farming sys- always produce positive results (Goulding tems can be improved. Improvements will et al., 2008). always be incremental, but that is to be A similar situation applies to another expected, given the inherent complexity of all important service provided by the soil biota: farming systems. regulation of soilborne pests and diseases. The essence of integrated soil biology There is plenty of evidence to demonstrate management is to manage agroecosystems at that biological mechanisms of suppression a farm and landscape level so that services operate in agricultural soils; that they act such as soil formation, carbon sequestration, against a wide range of pests and patho- nutrient cycling, water regulation and pest gens; and that they are influenced by man- and disease suppression are maximized and agement (Baker and Cook, 1974; Stirling, disservices such as nutrient runoff, sedimen- 1991; Hoitink and Boehm, 1999; Kerry, tation of waterways and greenhouse gas 2000; Weller et al., 2002; Stone et al., 2004). emissions are minimized. The issues involved Sometimes the suppressive agents are were depicted previously in Fig. 1.1 and dis- highly specialized antagonists, while in cussed by Power (2010) and Powlson et al. other cases suppression is associated with (2011a). Although the approach involves 94 Chapter 4

manipulating soil, crops and farm animals enhancing the activity and diversity of the to achieve the desired effects, the term ‘inte- soil biological community, farmers must grated soil biology management’ is used focus on adopting practices that increase total because the outcomes are manifested through carbon inputs, maintain labile carbon frac- the soil biota. tions in the rooting zone and reduce the rate Managing soil organic carbon is cent of decomposition of organic matter. Such ral to integrated soil biology management practices include rotational cropping, inter- because the quantity and quality of soil cropping with perennials, green manuring, organic inputs affect the activity and diver- residue retention, mulching and minimum sity of organisms within the soil food web, tillage. and they, in turn, influence numerous soil Since nutrient cycling/recycling is one properties relevant to ecosystem function of the ecosystem services provided by soil and crop growth. Since organic carbon levels organisms, plant nutrition is one of the key in many cropped soils have declined to the elements to be considered when attempts are point where agricultural productivity is made to manipulate the soil biological com- being compromised, practices that promote munity. Crop residues and organic amend- carbon sequestration are actively promoted ments are the only source of nitrogen and in the literature on sustainable farming other plant nutrients in low input and systems, and soil organic carbon is always organic farming systems, and their availabil- seen as a keystone indicator of soil health. ity to the crop is mediated by the soil biota. There is no particular critical threshold for However, in conventional farming systems, organic carbon that is applicable across dif- these natural decomposition and mineraliza- ferent soils and environments (see review by tion processes are largely overridden, with Loveland and Webb, 2003), but it is clear that crop nutrient requirements being supplied carbon levels in most agricultural soils are as mineral fertilizers. The challenge of inte- well below the maximum level attainable in grated soil biology management is to man- a given soil type and location. Raising total age carbon inputs so that biological processes carbon levels normally provides benefits, provide a greater proportion of the nutrients but as the above review indicated, the required by the crop. Instead of applying a ‘active’ or ‘fresh’ fraction seems to be more single pulse of fertilizer at excessive rates important in determining services associ- (because leaching or other losses are expected ated with soil structure and aggregation. later in the growing season), the aim would Since these fractions support the soil biota, be to develop better ways of utilizing the they are also the key to maintaining func- nutrients gradually made available from soil tions such as nutrient cycling and biological reserves, crop residues and biological nitrogen suppressiveness. fixation. The plants’ additional growth require The organic carbon content of a soil is the ments would be satisfied with judiciously placed result of a balance between inputs (plant and appropriately timed inputs of organic or roots, root exudates, plant residues and synthetic fertilizers at critical periods. manures) and outputs (evolution of CO2 due As we learn more about the organisms to respiration by the soil food web, leaching that provide these nutrient-cycling services, of soluble organic carbon compounds down and are more easily able to enumerate them the soil profile, and particulate losses from using molecular methods, this type of man- erosion). However, in the absence of substan- agement will become increasingly feasible. For tial inputs of manure or other organic mater example, in a series of studies cited by Ferris ials, it is difficult to influence these processes (2010), bacterial-feeding nematodes mineral- and increase the total organic carbon content ized nitrogen throughout the growing season, of arable soils. Nevertheless, this is a worth- but due to the different temperature adapta- while objective, as small changes in total car- tions of the nematodes involved, the nutritional bon content can have disproportionally large service was mainly provided by rhabditids in effects on a range of soil properties (Powlson spring and cephalobids in summer (Fig. 4.2). et al., 2011a). Thus, from the perspective of In another example, concentrations of mineral Global Food Security and Sustainable Agriculture 95

300 100 Functional continuity of N-mineralization by bacterial-feeding nematodes

Functional complementarity of N-mineralization Functional complementarity of N-mineralization by rhabditid nematodes by cephalobid nematodes 75 200

100 N-mineralization 25 Number of nematodes

0 0 Mar Apr May JunJul Aug Sep

Fig. 4.2. Functional continuity of nitrogen mineralization (based on lifetime mg N per individual) for diverse assemblages of rhabditid and cephalobid nematodes adapted to temperature conditions in California during spring (March–May) and summer (June–September), respectively. (From Ferris, 2010, with permission.) nitrogen available to a tomato crop were by this community have largely disap- enhanced by manipulating cover cropping peared from agricultural soils because the and irrigation practices to create conditions soil food web is repeatedly disrupted by suitable for biological activity, particularly cultivation; beneficial organisms are dis- bacterivore nematodes (Ferris et al., 2004). turbed or killed by pesticide and nutrient Since environmental conditions that favou inputs; vital food reserves are depleted red bacterivore nematodes probably also because carbon is exported as harvested favoured other microbial grazers, including product and not replaced; and decomposi- protozoa, the abundance of these nematodes tion processes that convert organic matter to was considered a useful indicator of overall CO2 are accelerated by tillage. Integrated grazing activity and nitrogen mineralization soil biology management means thinking rates from soil fauna. Therefore, both these holistically about all the practices used to examples suggest that identifying the key produce crops; recognizing that the sup- organisms responsible for nutrient-cycling pressive services provided by the soil food services and then manipulating their popula- web are affected by management; and then tions through management is a pathway to redesigning the farming system so that more sustainable nutrient usage. those services begin to operate effectively. One ecosystem service that has been This issue is explored in more detail in lost in modern agriculture is the capacity Chapter 11. of the system to suppress soilborne pests and diseases. Plant-parasitic nematodes and other soilborne pathogens normally do not cause problems in natural systems because they are kept under control by organisms Ecologically Based Management that compete with them for the same food Systems and the Role of Farmers resource, and by parasites and predators at higher trophic levels in the soil food It is easy to idealize that ecologically based web. This interacting biological community decision making should play a greater role in remains active and diverse because it is con- agriculture. However, achieving this in prac- tinually maintained by carbon inputs from tice will require mechanisms for dealing with plants. The suppressive services provided the complexity that is inevitably associated 96 Chapter 4

with production systems that rely heavily Implications for Biological Control on ecological processes. Shennan (2008) encapsulated the issues in this way: (i) in The first section of this chapter highlights the real farming systems, multiple variables fact that food security will be one of this cen- interact in site-specific and farmer-specific tury’s key global challenges. More food must ways; (ii) the outcomes of complex biotic be produced from existing resources without interactions can be unpredictable and idio- damaging the environment, and this will largely syncratic; (iii) crop-specific and site-specific be achieved through a process of sustainable knowledge, together with an understanding intensification. Those involved in agriculture of general system behaviour, is required to will continue to innovate, but proven tech- manage the whole system; and (iv) manage- nologies associated with conservation agri- ment complexity and perceived higher risks culture and site-specific crop management (relative to the continued use of chemical will form the basis of future farming systems. inputs) are a significant barrier to the wider Thus, in the foreseeable future, farmers in many adoption of ecological agriculture. It was countries face the challenge of introducing prac- also noted that discipline-based researchers tices such as reduced or zero tillage, cover are not well equipped to cope with this com- cropping, residue retention, crop rotation and plexity, as they study only a few variables site-specific management into crop produc- and try to control others in their attempts tion systems where such practices are not yet to understand the mechanisms driving eco used widely. Given the complexity of farming logical interactions. systems, together with the natural predisposi- Given the difficulties involved in tion of farmers to resist change, and the fact that managing ecologically based systems of many governments stifle innovation by subsi- agriculture, there is a need to consider dizing agriculture, this will not be an easy task. how growers can assimilate the knowl- Nevertheless, on-farm research sites must be edge that is generated by research and use established to demonstrate that farming sys- it to improve their farming systems. The tems can be modified, and agronomists and traditional approach to agricultural exten- extension personnel will need to work with sion has been to develop management rec- farmers to develop and then fine-tune the ommendations based on mechanistic new systems. Nematologists must be involved research and then extend them to farmers in this process, because the task of reducing in different growing regions. Shennan losses from nematode pests, and the problems (2008) argued that this research/extension involved in manipulating the free-living nema- model was no longer applicable and should tode community to improve nutrient cycling be replaced by an interactive learning and regulatory processes, are inextricably linked model involving farmers and researchers. to the development of crop and soil manage- This process would accommodate knowl- ment systems that improve soil health, increase edge held by both parties and should, productivity and enhance sustainability. therefore, result in two outcomes: far Once farmers begin to use variable- mers would increase their understanding rate-application equipment and other methods of ecological processes so they could better to optimize nutrient inputs, and crop moisture adapt management approaches to suit their stress is reduced by minimizing evaporative own situation, while researchers would losses, increasing the soil’s water-holding become more aware of the multiple varia- capacity and improving irrigation manage- bles that were interacting within a real ment, nematologists will have to address the farming system and could begin to con- issue of whether plant-parasitic nematodes sider how they might be responding to are still causing economic losses. Stress asso- management. The new model would be ciated with inadequate water or nutrient accompanied by an increase in field-based uptake exacerbates damage caused by nema- adaptive research, with an emphasis on todes (Barker and Olthof, 1976; McSorley monitoring performance as adaptations and Phillips, 1993), and so it is likely that were made. problems caused by nematodes will become Global Food Security and Sustainable Agriculture 97

less severe when these stress factors are ame- •• How does this vary with soil type and liorated or removed. Thus, estimates of the climate? severity of losses caused by nematodes (see •• Are particular forms or fractions of Box 3.4) may no longer be relevant, as they soil organic matter associated with were obtained in farming systems that in many suppressiveness? cases are markedly different to those operating •• What practices must be implemented to today. Crop loss estimates must, therefore, be maintain the continuity of regulatory redetermined under conditions where crops services? are grown in a more sustainable manner, and •• What suppressive agents are involved water and nutrients are managed using the and does their relative importance vary best available technologies. The critical ques- with crop, soil type and environment? tion to be answered is whether the optimization •• What easily measured parameters can be of crop management results in situations where used as indicators of suppressiveness? damage thresholds increase to a point where •• What is the impact of potentially disrup- plant-parasitic nematodes become a relatively tive treatments (e.g. tillage, nutrient minor constraint to crop production. All available inputs, pesticides) on suppressiveness? evidence suggests that nematodes will cause •• Are particular soil properties (e.g. clay con- fewer problems when environmental stresses tent) associated with suppressiveness? are minimized, opening up opportunities to •• What is the role of environmental factors manage them using strategies that focus on such as moisture and temperature? improving soil and plant health rather than •• Can organic inputs be manipulated to eliminating the pest. achieve higher or more constant levels of From an ecological perspective, the main suppression? benefit from introducing some or all of the practices associated with conservation agri- These issues are discussed later in this book, culture will be to enhance levels of soil organic but it will be apparent from the discussion in matter, particularly in surface layers. Given Chapter 9 that we have taken no more than a the role of soil organic matter and its associ- few small steps towards understanding how ated biota in improving soil moisture relations organic inputs influence natural regulatory and in storing and cycling nutrients, this processes in managed ecosystems. Organic improvement will have major flow-on effects amendments, for example, are often used as a to the crop loss/damage threshold issue dis- nematode management tool, but outcomes cussed in the previous paragraph. However, it are essentially unpredictable due to our lack will also affect the natural processes that regu- of knowledge of the chemical and biological late populations of nematodes and other soil- processes associated with the decomposition borne pathogens. Organic matter-mediated of organic matter. disease suppression is a widely recognized Complexity is a theme that runs through- phenomenon (Stone et al., 2004), and so levels out this book. Biological complexity is inevita- of suppressiveness should increase when soil ble when dealing with terrestrial ecosystems, as all is no longer tilled and growers begin to see org six kingdoms of life (Bacteria, Archaea, Protista, anic matter as a valuable resource rather than Plantae, Fungi and Animalia) occur in soil and something that interferes with farm opera- there is incredible diversity within each king- tions. The challenge facing nematologists is to dom. Since it is simply impossible for one per- understand how the quantity, quality and tim- son to be familiar with the taxonomic and ing of organic inputs, and how they are man- ecological attributes of all these organisms, soil aged, influence the regulatory processes that biologists tend to specialize. Thus, if science is stabilize populations of plant-parasitic nema- to ever come to grips with the complexity of the todes. There are many questions to be answered: soil biota, interdisciplinary cooperation must occur, and biologists working with soil must •• What level of soil organic carbon is have a broad understanding of soil ecology. required to achieve useful levels of When the complexity associated with suppressiveness? modern farming systems is added, it should 98 Chapter 4

be apparent that biological control of nema- Once those systems are in place, the stresses todes cannot be considered in isolation from associated with poor soil health should be the many other economic, environmental, minimized, while the mechanisms regula productivity and sustainability issues that ting nematode populations should start to affect the way crops are grown. It is for this function as a result of interactions between reason that integrated soil biology man plants, crop residues, the nematode commu- agement, rather than biological control, is nity and the environment. In many situa- emphasized throughout this book. Biological tions, no further steps will be necessary, control will only become a component of other than the ongoing process of steward- nematode management programmes if the ship, as nematodes will no longer be pests of interactions required to achieve it operate major economic concern. However, there within farming systems that are both profit- will also be situations where a particularly able and sustainable. Thus, the first step in virulent nematode pest is attacking a crop, establishing effective methods of biologic and in those cases, the level of nematode al control is to work towards developing control may have to be increased by fine- farming systems that provide a better biotic tuning the new farming system or introduc- and abiotic environment for growing plants. ing other management tactics. This chapter is from the book:

9781780643595.pdf

ISBN: 9781780643595 Contents

Contributors vii Preface x Acknowledgements xi 1 Introduction to Biosecurity Surveillance: Quantitative Approaches 1 Frith Jarrad

Part I Concepts for Biosecurity Surveillance 2 Biosecurity Surveillance in Agriculture and Environment: a Review 9 Megan Quinlan, Mark Stanaway and Kerrie Mengersen 3 Getting the Story Straight: Laying the Foundations for Statistical Evaluation of the Performance of Surveillance 43 Samantha Low-Choy 4 Hierarchical Models for Evaluating Surveillance Strategies: Diversity Within a Common Modular Structure 75 Samantha Low-Choy 5 Th e Relationship Between Biosecurity Surveillance and Risk Analysis 109 Alan MacLeod 6 Designing Surveillance for Emergency Response 123 Zoé van Havre and Peter Whittle

Part II Information for Biosecurity Surveillance 7 Th e Role of Surveillance in Evaluating and Comparing International Quarantine Systems 137 Murthy Mittinty, Peter Whittle, Mark Burgman and Kerrie Mengersen 8 Estimating Detection Rates and Probabilities 151 Cindy E. Hauser, Georgia E. Garrard and Joslin L. Moore

v vi Contents

9 Ad hoc Solutions to Estimating Pathway Non-compliance Rates Using Imperfect and Incomplete Information 167 Andrew P. Robinson, Matthew Chisholm, Robert Mudford and Robert Maillardet 10 Surveillance for Soilborne Microbial Biocontrol Agents and Plant Pathogens 181 Peter Whittle, Ingvar Sundh and Stephen Neate 11 Design of a Surveillance System for Non-indigenous Species on Barrow Island: Plants Case Study 203 Justine Murray, Peter Whittle, Frith Jarrad, Susan Barrett, Richard Stoklosa and Kerrie Mengersen 12 Towards Reliable Mapping of Biosecurity Risk: Incorporating Uncertainty and Decision Makers’ Risk Aversion 217 Denys Yemshanov, Frank H. Koch, Mark Ducey and Robert A. Haack 13 Detection Survey Design for Decision Making During Biosecurity Incursions 238 John M. Kean, Graham M. Burnip and Amin Pathan

Part III Statistical Modelling Methods for Designing Biosecurity Surveillance 14 Inference and Prediction with Individual-based Stochastic Models of Epidemics 253 Gavin Gibson and Christopher A. Gilligan 15 Evidence of Absence for Invasive Species: Roles for Hierarchical Bayesian Approaches in Regulation 265 Mark Stanaway 16 Using Bayesian Networks to Model Surveillance in Complex Plant and Animal Health Systems 278 Sandra Johnson, Kerrie Mengersen, Michael Ormsby and Peter Whittle 17 Statistical Emulators of Simulation Models to Inform Surveillance and Response to New Biological Invasions 296 Michael Renton and David Savage 18 Animal, Vegetable, or … ? A Case Study in Using Animal-health Monitoring Design Tools to Solve a Plant-health Surveillance Problem 313 Susan Hester, Evan Sergeant, Andrew P. Robinson and Graham Schultz 19 Agent-based Bayesian Spread Model Applied to Red Imported Fire Ants in Brisbane 334 Jonathan M. Keith and Daniel Spring Appendix: Common Statistical Distributions Used in Statistical Modelling and Analysis for Biosecurity Surveillance 348 Jessie Roberts, Samantha Low-Choy, Frith Jarrad and Kerrie Mengersen Index 363 Biosecurity Surveillance in Agriculture and Environment: 2 a Review

Megan Quinlan,1* Mark Stanaway2 and Kerrie Mengersen2

1Centre for Environmental Policy, Imperial College London, UK; 2Queensland University of Technology, Brisbane, Australia

2.1 Introduction: the Concept of (Zmorzynska and Hunger, 2008). In this Biosecurity context of agricultural and environmental biosecurity, defi nitions vary in detail but are Th e term biosecurity has many defi nitions. similar in intent at international, regional, It is frequently perceived as a new, more national and local scales. Defi nitions and coordinated approach, generally led by a commentaries from various sources are particular governmental authority or shown in Table 2.1. network of authorities, to understand and However, we commence the chapter manage natural and human-caused threats with a broader review of the defi nition of to a range of biological resources. Th e biosecurity and biosecurity surveillance to approach includes an ‘increasing reliance on clarify the usage of the term. Th e term has systematic risk analysis’ (FAO, 2007) and also been employed to mean a framework integration of existing sectoral capacities, for evaluation of introductions of living which consequentially highlights any gaps in organisms, including defence against bio- authority or coverage of risk management logical weapons and bioterrorism (O’Toole measures. Th e holistic, almost organic and Inglesby, 2003; Normann, 2010). Th e nature of the concept (for which the specifi c term appeared in publications about the objective or desired outcome may not always growing bioterrorist threat around 1995 be clear) is balanced against a pragmatic (Zmorzynska and Hunger, 2008). Its use in insistence on cost-eff ective, effi cient steps that context then expanded rapidly after the towards protection of valued resources. 2001 incident of bioterrorism of anthrax in In keeping with the theme of this book, postal letters. A 2006 report, ‘Globalization, the focus of this chapter will be on Biosecurity, and the Future of the Life biosecurity and biosecurity surveillance Sciences’ (National Research Council, 2006), among plants, animals and ecosystems. In defi nes biosecurity as ‘security against the this sense, the term biosecurity includes: (i) inadvertent, inappropriate, or intentional the protection of countries against alien malicious or malevolent use of potentially (non-endemic or non-native) plant, animal dangerous biological agents or bio- or marine pests (Waage and Mumford, technology, including the development, 2008); (ii) measures to contain or reduce production, stockpiling, or use of biological existing disease (Defra, 2005); and (iii) food weapons, as well as natural outbreaks of safety, sometimes known as food defence newly emergent and epidemic diseases’.

*[email protected]

Table 2.1. Biosecurity defi nitions and commentaries relevant to agriculture and environment. Organization or country Defi nition/commentary Reference Food and Agriculture Biosecurity is a strategic and integrated approach that FAO (2005) Organization of the encompasses the policy and regulatory frameworks United Nations (FAO) (including instruments and activities) that analyse and manage risks in the sectors of food safety, animal life and health, and plant life and health, including associated environmental risk. Biosecurity covers the introduction of plant pests, animal pests and diseases, and zoonoses, the introduction and release of genetically modifi ed organisms (GMOs) and their products, and the introduction and management of invasive alien species and genotypes. Biosecurity is defi ned as a holistic concept of direct relevance to the sustainability of agriculture, food safety, and the protection of the environment, including biodiversity. FAO paper on …‘harm’ is the damage done by something that might Cock (2003) biosecurity and have been prevented through biosecurity, whereas forests ‘risk’ is the chance of that harm occurring. FAO paper on farm Biosecurity plans require the adoption of a set of FAO (2011) (on biosecurity attitudes and behaviours that reduce risk in poultry) activities involving … production and marketing. A comprehensive, detailed, practical and easily understood plan is most effective. Windhoek Declaration … biosecurity … safeguards animal health, protects Windhoek Declaration on an aquatic biodiversity, promotes environmental sustainability (2009) biosecurity and enhances food safety. The livelihoods of many framework for people depend on fi sheries and aquaculture, southern Africa including some of the most vulnerable in the region. Australia Environmental biosecurity is the protection of the Australian environment and social amenity from the negative Government, effects associated with invasive species: including Department of weeds, pests and diseases. It occurs across the Sustainability, entire biosecurity continuum: pre-border Environment, Water, preparedness, border protection and post-border Population and management and control. Communities (2013) New Zealand … the exclusion, eradication or effect management of New Zealand risks posed by pests and diseases to the economy, Government, environment and human health. Ministry for Primary Industries (undated) Canada (dairy cattle) Farm-level biosecurity is a series of management CFIA (2013) practices designed to minimize or prevent and control: (i) the introduction of infectious disease agents onto a farm; (ii) spread within a farm production operation; and (iii) export of these disease agents beyond the farm that may have an adverse effect on the economy, environment and human health. Canada (beef cattle) Those practices that prevent or mitigate disease from CFIA (2012) entering, spreading within or being released from operations that may contain livestock. Biosecurity Surveillance in Agriculture and Environment 11

Organization or country Deﬁ nition/commentary Reference Bhutan Biosecurity shall contribute to achieving Gross Frampton (2010) National Happiness by ensuring Bhutanese people, the biological resources, plants and animals are protected from the harmful effects of pests and diseases, invasive alien species, genetically modiﬁ ed organisms, toxic chemicals and food additives. Tasmania Australia … the protection of industries, the environment and Government of public well-being, health, amenity and safety from Tasmania (2007) the negative impacts of pests, diseases and weeds. Victoria Australia … the protection of the economy, the environment, State Government of social amenity or human health from negative Victoria, Department impacts associated with the entry, establishment or of Primary Industries spread of animal or plant pests and disease, or (2010) invasive plant and animal species. Great Britain Biosecurity means taking steps to make sure that GB NNSS (2011) Non-native Species good hygiene practices are in place to reduce and Secretariat (GB minimize the risk of spreading invasive non-native NNSS) species.

Th e term is further convoluted through standing of the term do arise. As a result of translation: for example, in Chinese, French, the broad and changing usage of this term, German and Russian, the terms biosecurity there is controversy over what is ‘in’ and and biosafety translate into the same word. ‘out’ of the defi nition of biosecurity. Th is is despite the fact that, in English, Arguments exist about whether the concept ‘biosafety’ is frequently linked with labora- is ‘animal and plant biosecurity’ or simply tory safety and biocontainment when ‘biosecurity’ (see Box 2.1). Of course, the research involves hazardous materials (e.g. nature of, and positions on, this question, pathogens), or to frameworks for evaluation typically depend on the discipline base of of genetically modifi ed organisms (GMO). the proponents, as discussed throughout Either as biosafety or biosecurity, this usage this chapter. aligns with the World Health Organization Moreover, the intent of biosecurity (WHO) defi nition as the ‘protection, control seems always to be interdisciplinary or and accountability for valuable biological intersectoral, aimed at balancing multiple materials within laboratories in order to pre- objectives and based on a more holistic vent their unauthorized access, loss, theft, approach to protecting and using the misuse, diversion or intentional release’ biological resources of the place under (Secretariat of the Biological Weapons Con- consideration. Some defi nitions consider vention, 2011). One commentary suggests biological resources in terms of entire that including the plant and animal health ecosystems, populations of one species, issues under the rubric of biosecurity would individual organisms and down to the link these too closely to the mentality of genetic level. Many of the defi nitions of national security measures and make biosecurity instead implicitly refer to actions activities less transparent (Zmorzynska and or practices of monitoring or surveillance or Hunger, 2008). Th ese defi nitions focusing control measures, or on the risk and risk on threats to security through biological management or mitigation of the threats. In means are not explored in depth in this this instance, sometimes the pathway or chapter. mechanism for the threat to biosecurity is Even when narrowed down to the highlighted. agricultural and environmental usage of Frequently, factors that are not strictly biosecurity, major diff erences in under- biological are covered by the defi nitions, 12 Megan Quinlan et al.

Box 2.1. Is biosecurity about plant and animal health?

Arguments exist about whether the concept is ‘animal and plant biosecurity’ or simply ‘biosecurity’. In most cases when a biosecurity approach is adopted, plant and animal health will persist as distinct sectors, at both legislative and operational levels (FAO, 2007). Economically, animals are comparatively higher value investments per head but plants can impact equally on food security. Biological differences include the comparatively larger number of plant pests, the modes and states of transport or pathways for entry of the pests, the biosecurity treatments and the timeframe required for response to an outbreak. Historically, animal biosecurity is more established and more cohesive. Furthermore, under the existing system for animal health, for the large part, surveillance is aimed at detection of ‘notiﬁ able diseases’ of animals, which is a predetermined list of fewer than 50 well- deﬁ ned diseases or syndromes that may occur in livestock or poultry (OIE, 2013). This leaves the health of many animals (essentially all non-domesticated ones) outside the vision of surveillance (Convention on Biological Diversity (CBD) Secretariat, 2001a). In further recognition of the importance of the historic sectors for animal and plant health, the FAO Biosecurity Toolkit (FAO, 2007) emphasizes the concept of biosecurity as one of integration rather than harmonization of sectors. This means that biosecurity surveillance encompasses the existing approaches to surveillance, plus a more coordinated and comprehensive monitoring of organisms, which might not traditionally be covered by the national authorities for plant or animal health. The new approach, which addresses gaps in these historic sectors but also emphasizes a more coordinated strategic approach, has suggested to many that a new term and, in some cases, a new governmental entity with new authorities, is required to face today’s threats to biological resources. This now clearly includes genetic resources, resources of individual organisms and populations, as well as ecological systems.

such as economic and social issues. Th is Certainly, a common understanding of approach was taken up by smaller nations, surveillance of biosecurity is hampered by in particular, where limits in resources the broad uses and wide variation of demand an effi cient and coordinated public meanings for biosecurity. We consider, then, sector. Early examples of biosecurity the concept of surveillance in the traditional initiatives from the 1990s include Norway sectors for animal and plant health. (see Sandlund et al., 1996; Håstein et al., 2008), New Zealand (Froud et al., 2008; MAF Biosecurity New Zealand, 2009) and 2.2 Plant and Animal Health Belize (Government of Belize, 2000; FAO, Surveillance 2008; Outhwaite, 2010), all relatively small nations. 2.2.1 Historic authorities and approaches Spatial aspects of the defi nitions vary for plant and animal health surveillance (e.g. farm level, country level, etc.) or are not defi ned. Few pin down a time scale for the In the context of animal biosecurity, the concept. Th e emphasis seems to be on an major source of guidance is the World ‘approach’, ‘strategy’ and ‘attitude’ as much Organisation for Animal Health or OIE as on the actions to be taken, as laid out in (formerly the Organization International Table 2.1. Given the multisectoral nature of des Epizooties). Th e OIE is the inter- the concept, biosecurity cannot be defi ned in governmental organization for improving specifi c terms as a state of health and well- animal health worldwide (OIE, 2013). being, as one might defi ne clean air or Created in 1924, the OIE remains the potable water. Th erefore, many of the primary body for global coordination, with a defi nitions of biosecurity instead implicitly total of 178 member countries in 2013. It refer to actions or practices of monitoring or was also subsequently recognized as a surveillance or control measures, themselves. reference organization, with all of its Biosecurity Surveillance in Agriculture and Environment 13

standards being recognized by the World national level by the appropriate authority Trade Organization (WTO) through the in the national governments (i.e. the Agreement on the Application of Sanitary National Plant Protection Organizations), and Phytosanitary Measures (SPS). In the although surveillance programmes may context of plant biosecurity, guidance, also be regional or subregional, or (less primarily in the form of standards, is frequently) global (IPPC, 2012b). developed through the International Plant In plant health, surveillance is further Protection Convention (IPPC) and its 179 clarifi ed in the defi nitions in Table 2.2, contracting parties. Th e IPPC is an which, taken as a whole, identify who does international agreement on plant health, the surveillance, what is being monitored, deposited with the Food and Agriculture the time period and how data will be Organization of the United Nations (FAO) recorded. In plant health, as in animal and operating under its administrative health, surveillance is a critical component structure, now over 60 years old. Th e aim of of determination of the health status of the the treaty is to prevent the transboundary country (i.e. pest status – present or absent). spread of exotic pests of plants and plant Offi cial programmes are linked to inter- products, in order to preserve plant national recognition of the health status resources and facilitate safe trade (IPPC, (e.g. for animal diseases), which directly 2012a). aff ects the opportunities for trade. As with animal health (OIE, 2013), Surveillance can also be used to orient and plant health guidance is implemented on the inform control programmes or ensure the

Table 2.2. Defi nitions from the International Plant Protection Convention (IPPC) relating to surveillance. (From International Standards for Phytosanitary Measures (ISPM) 5; FAO, 2012.) Ter m Defi nition References Surveillance An offi cial process which collects and records data on CEPM (1996) pest occurrence or absence by survey, monitoring or other procedures Monitoring An offi cial ongoing process to verify phytosanitary CEPM (1996) situations Monitoring survey Ongoing survey to verify the characteristics of a pest FAO (1996) population Survey An offi cial procedure conducted over a defi ned period FAO (1990) (revised of time to determine the characteristics of a pest CEPM, 1996) population or to determine which species occur in an area Delimiting survey Survey conducted to establish the boundaries of an FAO (1990) area considered to be infested by or free from a pest Detection survey Survey conducted in an area to determine if pests are FAO (1990) (revised present FAO, 1996) Occurrence The presence in an area of a pest offi cially recognized FAO (1990) (revised to be indigenous or introduced and not offi cially FAO, 1996; ISPM 17; reported to have been eradicated (formerly ‘occur’) FAO, 2002) Pest record A document providing information concerning the CEPM (1997) presence or absence of a specifi c pest at a particular location at a certain time, within an area (usually a country) under described circumstances Pest status (in an Presence or absence, at the present time, of a pest in CEPM (1997) (revised area) an area, including where appropriate its distribution, ICPM, 1998) as offi cially determined using expert judgement on the basis of current and historical pest records and other information 14 Megan Quinlan et al.

effi cacy of risk management (preventative Alert List, a monthly bulletin of resources or control) measures, as noted in Box 2.2. and news, and a list of invasive alien plants) Th ese defi nitions are detailed and to facilitate the identifi cation of potential precise and establish the various aspects of pest risks (MacLeod, 2010). surveillance, which is a combination of For animal health, FAO carries out the targeted surveys and ongoing monitoring Emergency Prevention Scheme (EMPRES) to: (i) detect new introductions or incursions to address prevention and early warning of pests; (ii) delimit any occurrences which across the entire food chain, including are being contained; (iii) provide offi cial animal health, plant protection and food judgement of the pest status; and (iv) be the safety (FAO, 2013). On the regional level, basis for records. Th ese records, in turn, the European Food Safety Authority (EFSA) aff ect decisions regarding the risk from was established by the European Union (EU) international trade. Th e need to set in response to the food crises in the 1990s parameters of time and space is included, such as bovine spongiform encephalopathy without indicating the appropriate values. (BSE) and dioxin in food products (Deluyka While most of the surveillance actions and Silano, 2012). as defi ned in Table 2.2 are conducted by In earlier studies, regional and global national authorities, regional and inter- initiatives were considered critical, because national entities and programmes are national-level surveillance and advance alert crucial to successful surveillance. Figure 2.1 systems have often been weak (Convention showing Cuba’s national surveillance system on Biological Diversity (CBD) Secretariat, in plant health (taken from IPPC Secretariat, 2001b), despite the available international 2012), illustrates the range of inputs into a guidelines. Historically there has been a lack surveillance system more graphically. For of conclusive or com prehensive information example, pest alerts are a critical component about pest status (presence or absence) and of the overall surveillance programme. inadequate data management systems. Both the European and Mediterranean Emergency actions, coming before an Plant Protection Organization (EPPO) and organism is offi cially recognized (e.g. the North American Plant Protection nationally as a quarantine pest or inter- Organization (NAPPO), both Regional Plant nationally as a notifi able disease), were not Protection Organizations under the IPPC, always supported by legal authority and provide early warning systems (including an political will has had a signifi cant infl uence

Box 2.2. The importance of surveillance in biosecurity programmes.

Surveillance is considered one of the primary activities in any biosecurity programme. Three steps in a biosecurity programme have been proposed (adapted from Cock, 2003) as:

• Problem formulation: identifi cation of objectives, time frames and spatial boundaries; identifi cation and assessment of risks; agreement on roles and responsibilities; agreement on methodologies for each of the three steps; identifi cation of decision points and indicators of success; development of contingency plans to establish fi nancial, human and infrastructural needs and access. • Surveillance: biological monitoring of the targeted threat; general monitoring for unanticipated changes, such as development of invasiveness or contagiousness over time; system monitoring to ensure that the procedures for detecting a threat are functioning correctly and fulfi lling the purpose (the latter point may be considered part of management). • Management: implementation of the chosen response activities, such as for containment or eradication; evaluation of success over time and, in the event of failure, actions to redress or mitigate the situation. This relies on post-invasion surveillance to continually inform the management. Biosecurity Surveillance in Agriculture and Environment 15

Monitoring system

List of quarantine Compilation and pests and regulated analysis of non-quarantine pests information

Control programmes Pest alerts and survey plans

Diagnostic systems

• Records Training of Implementation •Reports technicians and according to area risks • Containment and producers control actions

Technology transfer

Fig. 2.1. The Republic of Cuba’s Phytosanitary Surveillance System [Sistema de Vigilancia Fitosanitaria en la República de Cuba] (as reported in IPPC Secretariat, 2012). on stopping trade (Convention on Biological animal health sectors. Th is has taken place Diversity (CBD) Secretariat, 2001a). through the global leadership of the OIE and IPPC, as well as FAO and numerous regional entities such as the InterAmerican Institute 2.2.2 Recent enhancements in plant and for Cooperation in Agriculture (IICA). It has animal health surveillance also been pursued by many of the national authorities. Some progress has been made Th e IPPC Secretariat discovered the through regular funding avenues, and other importance of the factors shown in Fig. 2.2, advancement has arisen from special which infl uence national pest surveillance, funding opportunities such as projects or in a recent survey of implementation of technical programmes. International Standards for Phytosanitary One example of advances from a Measures (ISPM) 6 (IPPC Secretariat, 2012). national initiative is a phytosanitary risk- Th e infl uence of such factors will be based rating for individual countries, magnifi ed in a biosecurity programme in developed by the United States Department most cases, unless the programme is of Agriculture/Animal and Plant Health established under new authorities with Inspection Service/Plant Protection and additional fi nancial and human resources Quarantine (USDA/APHIS/PPQ) Center for (the two highest priority factors identifi ed Plant Health Science and Technology’s in plant health surveillance). Plant Epidemiology and Risk Analysis Concurrent with the development of the Laboratory (CPHST PERAL) (USDA/APHIS, concept of biosecurity, several organizations 2010). have been working to enhance the use of risk A regional project to enhance pest risk analysis and management along with the analysis (PRA), nicknamed PRATIQUE and closely linked surveillance in plant and funded under the EU Framework Programme 16 Megan Quinlan et al.

100 90 87 80 73 70 60 59 50 37 40 35 30 24 23

Percentage (%) Percentage 20 20 16 12 10 4 0

Policy Training Financial Awareness Legislation Operational

Human resources

Information technology Geopolitical/environmental Equipment and infrastructure Cooperation and communication

Fig. 2.2. Priority areas affecting capacity to conduct effective pest surveillance (compiled from a survey by the IPPC Secretariat, 2012).

7, reviewed methodologies for the detection the global data bank. Any unusual or unclear of pests in trade and surveillance of exotic diagnosis is also confi rmed by a ‘chain of pests (Baker et al., 2009; Baker, 2012). A science’ that combines national and inter- major output of the project was a com- national expertise. Boa and Reeder (2009) prehensive review and rationalization of describe how this system had, by that year, various types of data available for pest risk produced 40 new disease records (NDRs), assessment, in particular, for Europe. confi rmed by the GPC and published in peer Th e intergovernmental treaty organ- reviewed journals, from 22 countries in ization CABI (www.cabi.org) is one of the Latin America and the Caribbean, Africa, leading sources of scientifi c expertise on Asia and Europe. Th is is, of course, in distribution and occurrence of pests, addition to the valuable advice for treat ment and an important source of taxonomic of previously known diseases and the identifi cation and diagnostics. Th e inter- confi rmation of distribution of these active databases for this information have diseases, for national and international greatly supported the national surveillance authorities. programmes. Over time, however, in addition to using literature review, informal and offi cial sources, a more novel source for 2.3 Characteristics of Biosecurity data has been developed. CABI is one of the Surveillance Programmes founding members of the Global Plant Clinic (GPC), now under the banner of Plantwise Surveillance plays an integral part in (www.plantwise.org), which has created a biosecurity programmes, as with animal and new paradigm for plant disease surveillance. plant health programmes, as indicated in Th is initiative has been accessing on-the- Box 2.2. Th e characteristics of surveillance ground observations through farmers’ programmes for biosecurity, in relation to queries at local market stalls, manned by those discussed in the section above, are GPC partners, which are then reported to outlined here. Biosecurity Surveillance in Agriculture and Environment 17

2.3.1 Integration of sectors 2.3.2 Broader participation

Challenges to surveillance, specifi cally the Public awareness contributes to monitor- detection, identifi cation and monitoring of ing eff orts and has been harnessed more animal, plant and even human diseases, systematically under the biosecurity were reviewed by a high-level Foresight approach (Convention on Biological programme in the UK to consider the likely Diversity (CBD), 2012). and possibly enhanced scenarios for 2015 Th ere is a growing body of literature on and 2030 (Offi ce of Science and Innovation, biosecurity surveillance as a distinct activity, 2006). Improvements in technology were within the broader domain of biosecurity considered key to addressing the increasing (Froud et al., 2008). For example, New threats in each fi eld. Limited resources Zealand defi nes biosecurity surveillance demand coordination to achieve any possible to be ‘the collection, collation, analysis, synergies (Barker et al., 2006), similar to the interpretation and timely dissemination of biosecurity approach. In the same information on the presence, distribution of programme, Quinlan et al. (2006) concluded prevalence or risk organisms and the plants from studies in the UK, sub-Saharan Africa or animals that they aff ect’ (Acosta and and China, that most of the challenges White, 2011). Th is defi nition itself has been would require integrated responses, with slightly modifi ed by the New Zealand sensitivities to culture and governance. Ministry for Primary Industries to be ‘an Some important areas for integration activity that occurs inside the border that is include standardizing approaches to data not part of an NPMS [National Pest collection and analysis, when cross com- Management Strategy]’ (as reported by Prime parisons are possible. A framework for risk Consulting International Ltd, 2002) and now assessment and estimates of impact of comprises four subcategories of surveillance: any type of regulated non-native species • Passive surveillance: the detection of (mammal, fi sh, insect, etc.), for example, exotic species through haphazard, was designed in the UK to facilitate decisions unplanned and unsolicited observations on priorities and feasibility for management by the general public, farmers, orchard- (Baker et al., 2007). ists, gardeners, veterinarians, plant Th is approach was presented in a case pathologists and others. study of the then newly formed Finnish Food • Enhanced passive surveillance: used Safety Authority (EVIRA) by FAO (2007), in situations where there is a requirement again emphasizing the need for integration, to improve the sensitivity of passive not harmonization. EVIRA reportedly surveillance processes through the maintained the key sectors as separate removal of barriers to the more detailed departments and accessed cross-cutting examination of situations in which expertise, such as risk assessment and particular pests might be present. communication, from departments external • Active surveillance: a planned process to theirs, but in the same Ministry. Other targeted to fi nd and identify a particular relevant Ministries provided policy input new pest. directly to EVIRA on a case-by-case basis. • Sentinel surveillance: uses targeted In the process of integration, however, groups of the population to monitor for a one must guard against restructuring specifi c pest or disease. without purpose and must support the transition over time. Th e Norwegian Food Examples are provided for each of these Safety Authority (2004) report on subcategories. Passive surveillance is institutional changes to the food safety illustrated by a person, working in the offi ce noted that: ‘In the aftermath of the fi rst of an industrial site, noticing strange wave of inspiration, one has identifi ed a caterpillars and sending them to an sense of personal loss.’ entomologist for identifi cation. An example 18 Megan Quinlan et al.

of enhanced passive surveillance is the community, depend on the actual pro- reimbursement of laboratory fees and the grammes undertaken and the scale of the payment of a sum to veterinarians operation. Th is is illustrated in Table 2.3. submitting material from cattle with clinical From the animal health and plant health signs that could possibly be associated with sectors, the concept of surveillance is to look BSE, or the use of publicity campaigns to for signs of diseases or pests (versus to encourage target groups to fi nd and notify determine the level of health or well-being, authorities of the discovery of any exotic per se, as one might when working for species. Active surveillance is illustrated by conservation of biodiversity). In that an active surveillance programme for fruit context, health, then, might be considered fl ies that might use pheromones in traps to high with the absence of detections of attract the target species. Th e example for diseases or pests, although proving a sentinel surveillance is bluetongue virus negative status of no disease is always harder surveillance in New Zealand, which involves than proving the presence of a disease. the regular testing of blood samples of cattle It is possible that some of the objectives from sentinel herds. for a good biosecurity programme are not In addition to governmental support of easy to articulate, as they may evolve and public participation in surveillance, par- appear as part of the process of discovery in ticipation from interest groups may enhance the new paradigm of cooperation. biosecurity. Th e International Union for the Conservation of Nature (IUCN) has an Invasive Species Specialist Group (ISSG), 2.3.4 Cultural shifts towards which comprises almost 200 members from collaboration and synergy over 40 countries and ‘aims to reduce threats to natural ecosystems and the native species Cook et al. (2010) discuss adaptive they contain by increasing awareness of governance as needed for invasive species invasive alien species, and of ways to which lie outside the historic division of prevent, control or eradicate them’ (www. animal and plant health. Some entire issg.org). Th e IUCN provided expert analysis categories of disease and pests have passed and advice for marine invasive species through the metaphorical ‘net’ even when biosecurity plans in a cooperative agreement potentially covered by a public authority. with the US Environmental Protection Th is was the case with multiuse woody Agency (US EPA) (Waugh, 2009) and has species and new sources of forage introduced worked with other governments in many in the 1980s, shrimp disease and diseases instances. introduced through fi sh stock (Murray and Peeler, 2005), serious aquatic weeds in the fi rst decade of 2000, and several severe tree 2.3.3 Additional drivers and pests over the past decade (Brasier, 2005). objectives Although some of these were addressed by existing authorities, the responses were Outbreaks of plant and animal pests occur reactive and of limited impact. for a variety of reasons. In the case of animal A major obstacle is the lack of biosecurity, some of these include human- information about new threats to bio- assisted movement of pests and pathogens, security. Even as a threat is identifi ed, the range extension of vectors and new vectors probabilities surrounding its occurrence and (Waage and Mumford, 2008), whether possible economic consequences make the intentional or by accident. decision process diffi cult and seemingly Th ese drivers provide the motivation for indefensible. Cook et al. (2010) make the biosecurity surveillance. Th e aim of the bold statement that: ‘In the face of activities undertaken as part of biosecurity uncertainty and ignorance, eff ective risk surveillance, and the corresponding benefi ts management requires that institutions of these activities to the industry and change their behavior in response to new Biosecurity Surveillance in Agriculture and Environment 19

Table 2.3. Aims and benefi ts of biosecurity and biosecurity surveillance. Organization/ country Aims and benefi ts of biosecurity surveillance Reference Victorian ..it ‘develops policy, standards, delivery systems and services that State Department reduces the threat of invasive plants and animals to agriculture and Government of Primary the natural environment, protects animals and plants from pests of Victoria, Industries and diseases, enhances food safety, ensures minimal and effective Department chemical use, protects the welfare of animals and preserves and of Primary expands market access for Victoria’s primary industries’. Industries (2010) Western Benefi ts of biosecurity: Government of Australia • minimization of the risk of exotic diseases and agricultural pests; Western DAF • eradication of diseases; Australia, • minimization of costs to producers by keeping pests, diseases and Department weed out of the State; of Agriculture • increased access to markets by ensuring that produce is as free as and Food possible from pests and chemicals; and (2010) • customer confi dence in clean, safe products.

New Zealand Post-border surveillance is undertaken for a variety of reasons, some MAF Biosecurity of the most important being: New Zealand • to give evidence that a pest or disease is absent from a country, (2009) region or defi ned area, thus enabling access to particular export markets; • to detect new pests and diseases early enough to enable cost- effective management; • to establish the boundaries of a known pest or disease incursion; and • to monitor the progress of existing containment or eradication programmes. Canada Looking beyond the direct economics of disease reduction, the CFIA (2013) (animals) benefi ts of implementing on-farm biosecurity practices are signifi cant. For producers, they include: • improving animal health and welfare; • keeping out new diseases; • cutting the cost of disease prevention and treatment; • reducing the use of medication, such as antibiotics, with an associated reduction in the risk of emergence of resistant pathogens; • producing safe, wholesome, and high-quality products; • increasing consumer and buyer confi dence; • protecting human health; • minimizing the potential for farm income losses; • enhancing the value of the herd; and • maintaining and accessing new markets for genetics. A Biosecurity Plan provides overall benefi ts to the dairy industry in that it: • decreases economic losses from some diseases that cannot be treated or controlled using vaccinations or other management strategies (e.g. mastitis, Johne’s disease); • helps to prevent the introduction of foreign diseases; • controls the spread of infection from region to region and farm to farm; • facilitates early recognition of emerging disease threats; • prevents zoonoses; • produces safe wholesome milk and meat; • negotiates more favourable global trade policies; and • maximizes genetic export markets by the prevention of disease. 20 Megan Quinlan et al.

understandings about how the world • making better use of existing data; operates.’ Th ey argue that rather than the • focusing monitoring better; and pre- to post-border continuum, biosecurity • ensuring that the mandates and re - must rely on active networking across all sources of key organizations match the nodes of data collection, analysis and policy need. formulation and risk management. Th e shift towards biosecurity may require additional expertise and resources to 2.4 Biosecurity Surveillance support a consultative and iterative Activities approach, such as for increased communi- cations. Greater agility and responsive ness, Agricultural and environmental biosecurity as well as the willingness to incorporate new surveillance programmes include both information, is part of the changes needed legislative and collaborative programmes (Cook et al., 2010). Th e hallmark of a good operating at multinational, regional, national biosecurity programme is the ability to and local levels. Th e growing importance understand, ‘live with’ and, at all oppor- of biosecurity both conceptually and tunities, address the uncertainty and lack of operationally has meant that it is now not information typical of these topical areas and only a priority of government agencies, but previously lost in legislative gaps, or left also a political priority. Th is is refl ected in the unaddressed due to resource limitations. appointment of Ministers for Biosecurity Th ese cross-sectoral interactions (e.g. New Zealand, Australia, Bhutan, the provide greater opportunity for replicating Gambia), the emergence of national bio- success ful strategies or methodologies in security strategies (New Zealand, Australia) one sector, to another. For risks to and the development of biosecurity aquaculture resources, Murray and Peeler legislation (e.g. New Zealand, Fiji, Samoa) (2005) created a framework combining risk- (Frampton, 2010). Many countries have analysis methods and virulence theory with national legislative and agency programmes historical examples (mainly from salmonid for biosecurity surveillance. In the context of pro duction) to identify key disease- plants, examples include USDA/APHIS emergence risk factors. Th ey proposed (USDA/APHIS, 2013), Biosecurity Australia treating hatcheries and slaughterhouses and (Biosecurity Australia, 2007), the New other points of possible cross contagion, Zealand Ministry for Primary Industries with strict biosafety-type procedures for (New Zealand Government, Ministry for pre vention of disease emergence. Primary Industries, undated), the National Biosecurity Commission and Biosecurity Policy of the Kingdom of Bhutan (Frampton, 2.3.5 Systematic analysis of risks and 2010) and so on. risk management Th e scale of operation of agricultural and environmental bio security surveillance We have already touched on the inherent programmes may be defi ned by the area need for systematic analysis as a cornerstone where a disease or pest outbreak has been to biosecurity, and the following sections contained, or conversely, an area free from elaborate this theme. the outbreak, or it may be defi ned by the Th e lack of ongoing surveillance of wild area of importance to the stakeholders, such populations of animals is considered a as protected areas, national parks or areas of serious weakness to the early alert of new high biodiversity (hot spots) or genetic human diseases, because so many new centres of origin. epidemics arise from zoonoses (Offi ce of A number of research organizations Science and Innovation, 2006). Th is study in and a wide range of individual researchers future synergies between human, animal have focused on these issues. Two such and plant surveillance names three research groups include the Australian principles for improvement: Centre of Excellence for Risk Analysis Biosecurity Surveillance in Agriculture and Environment 21

(ACERA; www.acera.unimelb.edu.au) and CRC has four main programmes focusing on: the UK-based Food and Environment (i) tools, technologies and strategies for Research Agency (FERA; www.fera.defra. early warning of new and emerging plant gov.uk), formerly Central Science pest threats; (ii) monitoring and surveillance Laboratory (CSL). for eff ective detection and response; (iii) FERA’s key areas of statistical capability safeguarding international trade and include uncertainty, modelling and risk managing estab lished pests; and (iv) assessment. Th e types of activities listed by working with community, government and FERA include: (i) wildlife rabies contingency industry to safeguard Australia for a secure modelling for use in an outbreak; (ii) future. modelling potential badger management A similar CRC was created in Australia to strategies for the reduction of bovine address animal biosecurity. Th e three tuberculosis in cattle herds in England, programmes of the CRC were Technologies Wales and Northern Ireland; (iii) a computer to Enhance Detection, Ecology of Emerging simulation study to evaluate resistance- Infectious Diseases, and Advanced Sur- delaying control strategies with novel veillance Systems. Th e key highlights of the anthelmintic products on UK sheep farms; Advanced Surveillance Systems programme and (iv) modelling European foul brood in included: (i) the development of an internet- the honeybee. based epidemiological calculator for In addition to a comprehensive set of estimating disease prevalence from pooled reports that contribute substantially to prevalence (www.ausvet.com.au); (ii) a knowledge and practice of statistical bovine syndromic surveillance system (www. modelling, design, and risk and uncertainty ausvet.com.au); (iii) a new sugar ‘lure’ for in environmental biosecurity, ACERA also mosquitoes; (iv) software that analyses has a focus on the elicitation of expert disease surveillance data to provide an information and the incorporation of this estimation of a country’s confi dence in information into risk assessment (Burgman, freedom from disease (www.ausvet.com.au); 2005; Low Choy et al., 2009). and (v) an electronic system for linking Large national programmes that address livestock movements to property data using agriculture and environmental biosecurity the National Livestock Identifi cation System have also been established. An example is the (NLIS). Australian Cooperative Research Centre (CRC) on National Plant Biosecurity (NPB) which was established in 2005 and renewed 2.5 Statistical Issues and Approaches in 2012. Th e CRC comprises around 25 in Biosecurity Surveillance entities drawn from government, research organizations, universities and industry groups. Th e original CRC produced a number Th is book focuses on statistical issues and of web-based applications, three of which corresponding statistical approaches to are: (i) the Plant Biosecurity Toolbox, which biosecurity surveillance. In this chapter we provides detailed diagnostic infor mation provide an overview of some of these issues (biology, taxonomy, detection, identifi cation) as a prelude to the more detailed discussions about exotic pests and diseases; (ii) the Pests that follow. and Diseases Image Library (PaDIL) which Many of the key statistical issues can be provides high-quality image and information described under three broad headings: tools to facilitate research and management • Modelling: building models to describe in biosecurity and biodiversity; and (iii) the and predict pest introductions, spread Remote Microscope Network (RMN) and outbreaks. (Th ompson et al., 2011) system, which links • Design: designing surveillance profi eld offi cers with national and international grammes, determining necessary survey experts to speed up the identifi cation of eff ort, optimal allocation of resources in potential biosecurity threats. Th e renewed surveillance and response. 22 Megan Quinlan et al.

• Risk and uncertainty: characterizing information drawn from a range of sources risk and uncertainty in these model- including observations, literature, expert based descriptions and predictions. judgement, and so on. Th e quantifi ed model then allows an assessment of the overall A range of approaches have been used to probability of the outcome (e.g. probability underpin the statistical models suggested of pest freedom), identifi cation of major for agricultural and environmental bio- factors contributing to the outcome and security surveillance. Th ese range from scenario (‘what if’) assessment (Johnson control charting techniques (Fox, 2006) to and Mengersen, 2012). BNs are currently hierarchical models (Stanaway et al., 2011) being used for pest risk management in the and systems models (Mengersen et al., Beyond Compliance project, an international 2012). project based in South-east Asia (Mengersen Control charts can be used to monitor et al., 2012). processes such as counts of pests or pest Th ere have been a variety of approaches presence/absence, or related measures of to biosecurity surveillance design. Th ese interest such as time to detection. Th ey include designs constructed to meet specifi c provide signal or alert systems if the process constraints (Barrett et al., 2009; Hester exceeds a predetermined threshold or et al., 2012), simulation-based approaches exhibits non-random patterns. Potential (Potts et al., 2012) and model-based reasons for the signal can then be designs. investigated. Th e broader range of quality Constraint-based surveillance designs, monitoring techniques can also be used to also sometimes known as risk-based designs, determine the capability of a surveillance ensure conformance to specifi c requirements system to meet specifi ed requirements. An such as a cost threshold or a guaranteed example of their use is for syndromic power to detect a species if it is present. An surveillance and anomaly detection (Fox, example of such a design for detecting the 2006). introduction of exotic plant and animal Hierarchical models allow the explicit pests on Barrow Island in Australia is description of observation-level and process- provided in Chapter 11, this volume. level characteristics of pest introduction, Software such as EpiTools (Sergeant, 2009) spread or outbreak. An example of this is a can also be used for this purpose, as Bayesian model for surveillance of spiralling demonstrated in the design of a surveillance whitefl y in Australia (Stanaway et al., 2011), system for citrus canker in the Northern in which surveillance and ecological Territory of Australia (Hester et al., 2012). information are used to estimate invasion Th is tool can also be used for animal extent and model parameters for invading surveillance designs, for example to estimate plant pests spread by multiple dispersal disease prevalence or demonstrate freedom modes, in particular by people. Th e model from diseases in animal herds (Sergeant, explicitly incorporates uncertainty in the 2009). observation process by allowing for local Simulation-based approaches can natural spread and population growth provide a way of evaluating the potential within spatial units. outcomes of a proposed surveillance design, Systems models typically take a broader such as the predicted risk of non-detection, perspective of the biosecurity surveillance pest spread or outbreaks. Th e simulation process. A Bayesian network (BN) is a form models are also for evaluating the impact of of systems model that has been increasingly diff erent design assumptions. Th e effi cacy of widely used in biosecurity. A BN is a type of this approach has been evaluated for the graphical model that describes the factors citrus canker surveillance problem that impact on or are associated with a mentioned in the previous paragraph. response of interest (such as absence of a Many of the approaches described above pest), and their (often complex) interactions. are discussed in more detail in subsequent Th e model is then quantifi ed, often using chapters of this book. For specifi city here, Biosecurity Surveillance in Agriculture and Environment 23

we focus on a review of a range of statistical the suspension of access to international modelling approaches to agricultural and and domestic markets until the extent of the environmental biosecurity surveillance. incursion can be demonstrated. Area freedom surveillance aims to provide suffi cient evidence to satisfy the importing 2.6 Statistical Modelling Approaches markets that the probability of moving the pest through trade from particular areas is 2.6.1 Statistical requirements low (Aluja and Mangan, 2008; Plant Health Australia, 2010). Guidelines for establishing Biosecurity aims to manage the risks of areas of low pest prevalence have recognized invading arthropod and disease pests by that area freedom is not a necessary carrying out pre-border, border and post- requirement for market access negotiations border control activities. Mitigation of risks (IPPC, 2008; Lloyd et al., 2010). However, is a bioeconomic management issue and the they have rarely been implemented due to strategic decision-making process has concerns over ecological (and operational) benefi ted from modelling both the uncertainty within quarantine systems probabilities and the consequences of pest (Aluja and Mangan, 2008). invasions (Myers et al., 1998; Cook, 2005; Delimiting extent is not only necessary Waage and Mumford, 2008; Carrasco et al., for maintaining trade but is also needed for 2010a,b; Epanchin-Niell and Hastings, managing eradication or long-term con- 2010). Ideally, risks are managed before tainment programmes (Cacho et al., 2010; pests breach the border but once an Carrasco et al., 2010c). Ongoing surveillance incursion has occurred, the task becomes provides information about the extent of one of eradication, minimizing spread or pests over time so that movement reducing the consequences in invaded areas. restrictions and control measures can be From a tactical point of view, post-border regulated most eff ectively. Each of these management of incursions requires spatial applications requires the spatial extent of inference to manage pests at an operational the pest to be reliably estimated over time level. Post-border surveillance provides the (Cacho et al., 2010). While inference on the data used to infer the likely extent of probability of pest extent provides the invading pests over time so that regulators foundation for decision making, the spatial can confi dently manage movement pathways statistics for analysing the dynamic extent and pest control strategies. of invaders are generally not available to the Post-border surveillance activities that agencies that manage incursions. feature in plant biosecurity risk management Th e initial design of any biosecurity include early detection, area freedom and investigation needs to consider the spatial response surveillance (McMaugh, 2005). units used for decision making, data Early detection surveillance aims to detect collection and ecological modelling (Graham pests in an area before they become too et al., 2004). In continuous space, a bounding widespread to eradicate (Hulme, 2006). polygon can be constructed around a Th ese programmes target surveillance at population. For incursions, where non- areas with a predetermined high probability contiguous satellite populations are com- of a pest being present (Wotton and Hewitt, mon, some meaningful ecological or 2004; Stark et al., 2006; Hadorn and Stark, management resolution is needed to defi ne 2008). Managers are interested in how to the functional boundaries (Burgman and best deploy early detection surveillance over Fox, 2003). More commonly, species space and time, while balancing the cost of distribution models seek to assign a value surveillance against the expected benefi t of for presence or absence to discrete cells. timely eradication or control (Myers et al., Th ese cells may be arranged on a continuous 1998; Prattley et al., 2007). regular grid (Argaez et al., 2005; Royle et al., Once an exotic pest is detected, the 2007) or may consist of an irregular patch- major economic threat facing producers is work (Gumpertz et al., 2000). 24 Megan Quinlan et al.

At fi ne resolutions, the eff ective extent one of estimating the hidden or latent extent of an invading plant pest is restricted to at a particular time (Clark, 2005). Typically, those individual hosts that are capable of visual inspection of hosts backed up by sustaining the pest throughout its life cycle. diagnostic tests provides the data, which are Hosts may be logically arranged for the used to demonstrate that areas are pest free. purposes of analysis into fi elds, farms or However, these data are far from complete. other landholdings. Alternatively, arbitrary Th e sites or areas to which observations of areas may be related to pest habitat based on presence or absence are attributed may only the density of hosts. Environmental be partially examined and even at a single constraints, such as weather conditions and plant scale, pests may be overlooked if the soil types that operate at broader scales may symptoms are not apparent to the observer also be used to restrict the area at risk. As (Bulman et al., 1999; Fitzpatrick et al., 2009; host landscapes are all fragmented on some Gambley et al., 2009). In order to infer the scale (With, 2002), it may be necessary to probability of pest absence for an area, an break the spatial domain down into observation process must be modelled to discontinuous habitat patches for a accommodate potential false absence particular analysis (Leung et al., 2004; records that apply to the spatial unit of Moilanen, 2004). Statistics that estimate interest (Kery, 2002; Tyre et al., 2003; Meats the extent of an incursion need to and Clift, 2005). accommodate the choice of spatial scale on If a pest is present in an area, false two fronts. First, the model outputs need to absence records are, to a large extent, be at a spatial resolution that is useful for dependent on the density of the pest making management decisions. Secondly, population in that area (Royle and Dorazio, models that include invasion ecology must 2006; Kery et al., 2006; Cacho et al., 2010). be at a resolution that can adequately Observation models alone can only be used represent the dynamics of spread over time. to provide evidence against presence at a Th e choice of a geographic model is therefore particular population intensity. It is the loss integral to the modelling process and the of power for observations to detect pests at parameterization of these models. low levels that challenges the delimiting of Ultimately, the managers of invading pest extent (Delaney and Leung, 2010). To pests seek to map the probable spatial extent infer pest absence in an area, additional of a pest at the current time (or at some time information about a pest’s likely intensity in the future) based on all of the information must be introduced into the analysis. available. Th ese maps can: (i) defi ne con- Information about pest intensity needs to tainment lines for pest control (Plant be derived from the particular reproductive Health Australia, 2010); (ii) help negotiate and spread characteristics of a pest. access to markets for produce from areas Statistically, this is expressed by the in - considered free of pests (Jorgensen et al., trinsic spatial and temporal correlation 2004; Martin et al., 2007; Lloyd et al., 2010); within a pest population (Wintle and and (iii) be used to deploy surveillance Bardos, 2006). Dynamical models for the resources to maximize the information invasion process can mathematically specify required to make decisions (Prattley et al., spread mechanisms (and parameter 2007; Barrett et al., 2009; Davidovitch et al., uncertainty) to allow structured ecological 2009). Biosecurity programmes generally information to be incorporated into the seek to simplify the population char- statistical analysis (Gibson et al., 2006; acteristics of an incursion into the presence Hooten et al., 2007). or absence of pests over space and time. Inference on the geographic distribution Even low populations of a pest represent a of an invading pest over time is operationally threat to the future management of an impossible without combining information incursion. As the location of each organism from observations and the ecology of the comprising the invasion is not known, the pest. Observational data collected by process of delimiting the extent becomes surveillance for diff erent pests could have Biosecurity Surveillance in Agriculture and Environment 25

quite diff erent interpretations for manage- observation model (MacKenzie, 2005). Th e ment depending on the reproduction and analyst must be mindful of the relationship dispersal dynamics of the organisms. between the outcome recorded, the latent Similarly, while the distribution of a pest state inferred and the eff ect of spatial is governed by its intrinsic ecology or aggregation of information within the epidemiology, quite diverse incursion model components. scenarios could unfold, given any particular Th e probability that a pest is observed introduction event. It is the role of within a site can be considered a function of biosecurity surveillance to tie the process of the search intensity (e.g. plants inspected, invasion to the landscape so that appropriate time spent, area covered) and the expression management decisions can be made. of the pest within the sampling frame (Kery, Quantitative modelling of surveillance data 2002). Consider a pest that is present on a and invasion dynamics provide a way particular number of plants at a site and is forward to assimilate this information and perfectly observed. If the proportion of embed it into biosecurity decision making. plants inspected from the area is relatively small, the probability of not detecting the pest may be adequately modelled by the 2.6.2 Pest observation models binomial distribution. Under the assumption that the plants selected are exchangeable, Statistical interpretation of biosecurity sur- this model can be used in the frequentist veillance requires an observation model form to arrive at a confi dence level for a that describes the imperfect signal that an predetermined prevalence (Cannon and observer receives about the true pest Roe, 1982). If the proportion of plants population when visiting a site. Traditionally, inspected is large, the observation model surveillance focuses on the visual inspection may instead be based on a hypergeometric of hosts or sampling of material, but similar distribution (Cameron and Baldock, 1998; models can be applied to other signal Hanson et al., 2003). Where the measure of detection data such as background passive search intensity is the proportion of the area surveillance (Cacho et al., 2010), trapping surveyed, or search time, a Poisson (Barclay and Hargrove, 2005; Meats and distribution provides a further option. Th ese Clift, 2005) and remote sensing (Wang, basic statistical functions for modelling 2009). In most plant health surveillance count data from observations can be systems, false positives are unlikely and so implemented in frequentist analyses or they observation of the pest (and subsequent can be used to provide the likelihood diagnostic confi rmation) is considered component of a Bayesian approach (Hanson suffi cient evidence that it is truly present. et al., 2003; Johnson et al., 2004). Th erefore the primary goal of observation Imperfect examination of those units models in plant biosecurity applications is that constitute the measure of search to analyse evidence for pest absence at a site. intensity is commonly referred to in the Biosecurity surveillance data typically epidemiology literature as test sensitivity consist of observational outcomes, generally (Cannon, 2001; Bohning and Greiner, 2006; presence/absence, attributed to a geographic Gambley et al., 2009) and in ecological area that is usually referred to as a site. Th e studies as detectability (Wintle et al., 2005; spatial defi nition of a site is somewhat Royle, 2008). Overestimation of detectability arbitrary, where the area may consist of a will result in underestimates of pest single plant, a fi eld, a farm or some other distribution that can severely compromise functional management area. A site may be population management decisions (Myers et subdivided into counted units that are al., 1998; Wintle et al., 2004). Th e simplest assumed to be independent and identically approach to imperfect detection is to use a distributed so that standard statistical point estimate of detectability to reduce the models can be applied. Th e spatial defi nition search intensity in the observation model of a site is integral to the construction of the (Martin et al., 2007). 26 Megan Quinlan et al.

Detectability on an infested unit may be by specifying a prior distribution on the infl uenced by a number of factors, for hyperparameters for overdispersed models instance, observability due to tree archi- or for random eff ects and parameters in tecture (Gambley et al., 2009), terrains logistic regression. Priors may be derived (Hauser and McCarthy, 2009) or diff erences from plausible values provided by experts, in observer experience (Gambley et al., 2009; or from existing empirical evidence (Hooten Christy et al., 2010). Variation in individual et al., 2007). pest behaviour may also result in mixtures In addition to uncertainty about of detectability (Royle, 2006; Christy et al., detectability, it is also necessary to consider 2010), as can spatial clustering on units the potential expression of the pest in the within the site (Gschlossl and Czado, 2008). context of the invasion process. A major Where there is epistemic uncertainty source of variation in detectability will be surrounding the detectability parameter, or the size of the population within the detectability is expected to vary between observation unit (Royle, 2006; Harwood et units, the data can be treated as being al., 2009). As an area is invaded, both the overdispersed (Potts and Elith, 2006). Th e number of infested units and the probability beta-binomial distribution is one analytically of detection on individual units will increase. tractable form for estimating detectability At the margins of the range, pest expression in a Bayesian framework that has led to its is expected to be poor and therefore models widespread use (Clark, 2003; Gelman et al., will lack inferential power (Barrett et al., 2004; Th ebaud et al., 2006; Hooten et al., 2009). Th e evidence for absence used for 2007). Data from overdispersed Poisson mapping extents is therefore sensitive to the processes may likewise be modelled using a way in which the observation model negative-binomial distribution (Royle, 2004; processes the pest signal at low population Gschlossl and Czado, 2008). levels. Another class of models for dealing with Pest observation outcomes recorded at overdispersion in presence/absence analyses some point in space and time are generally are the zero-infl ated binomial and zero- interpreted as applying to some spatio- infl ated Poisson models (Hall, 2000; temporal vicinity (Yoccoz et al., 2001). Branscum et al., 2004; Wintle et al., 2004; Observations taken at a site at one time are Martin et al., 2007). For pest count data in a expected to refl ect the true status at times in binomial setting, the models consider the the recent past and future. Temporal outcomes of the observation process to be discounting of surveillance data has been either zero or binomial depending on the examined for herd-based sampling in pest status. Royle (2006) recommends veterinary epidemiology given continued caution when using zero-infl ated models to exposure to infection (Schlosser and Ebel, infer population sizes at low densities. 2001). In a similar way, observations in one Th erefore, despite their simplicity, these area are expected to contain information models may have limited value in estimating about nearby or connected areas. pest absence for biosecurity applications. Autocorrelation of the pest status in Most biosecurity surveillance programmes space and time is a function of the invasion are limited to the collection of presence/ ecology of the organism. It is recognized absence data, suggesting that logistic that the assumptions required of simple regression models to predict the status of inferential probability models are usually sites are given some additional covariate violated in the face of spatial autocorrelation data such as host status or environmental (Legendre, 1993; Wintle and Bardos, 2006). favourability (Kery, 2002; Gelman et al., To delimit extent, the observation process 2004). must be modelled in relation to internal In a Bayesian setting, the foundation processes within the observation unit, but observation models discussed so far provide this must also be supported by the external the likelihood function for analysis. processes that give rise to interdependencies Uncertainty in detectability can be defi ned with other units. In the following section, Biosecurity Surveillance in Agriculture and Environment 27

invasion process models are introduced to IPPC adopts the terminology of endangered defi ne some ecological processes that give areas to identify a region that favours the rise to spatial and temporal correlation. establishment of a pest of concern, while establishment is defi ned as the perpetuation of a pest in an area for the foreseeable 2.6.3 Invasion process models future (FAO, 2012). Here we consider the colonization process as applying to any area General reviews on invasion ecology can be of interest for which the pest status is found in Mack et al. (2000), Puth and Post sought. Th e process encompasses the intro- (2005), Liebhold and Tobin (2008), duction of the pest into the area, followed by Simberloff (2009) and With (2002). Th e successful reproduction and leading to spatial realization of an invasion process permanent establishment. Considerable over time is the result of the birth, dispersal work has gone into identifying the intrinsic and death of many individual organisms. As biological characteristics of successful the extent of an invasion evolves as a invaders (Johnson et al., 2006). However, dynamic process, considerable heterogeneity the most reliable indicators of invasion and spatial dependence is displayed in the success across taxa appear to be extrinsic distribution patterns (Hastings et al., 2005). factors such as climate/environment Spatial correlation can be due to similar similarity and the number of pest propagules underlying environments as well as being introduced (Jarvis and Baker, 2001a; Rouget intrinsic to the dispersal process itself and Richardson, 2003; Hayes and Barry, (Wintle and Bardos, 2006). Th e probability 2008). of a pest being present in a particular Habitat suitability, in particular the area can be modelled as a function of availability of suitable host plants and the dispersal-mediated connections with climatic requirements, has a major impact infested sites and the time over which those on the probability that an area will be connections exist (Jerde and Lewis, 2007). colonized. Climate matching has proved to Invasion processes can be broken down be one of the most useful estimators for the in diff erent conceptual ways, depending on ultimate distribution of an invading the components of interest to particular organism (Sutherst and Maywald, 1985) but applications (Simberloff , 2009). Component comes with some caveats. Biogeographic processes of interest can include introduction predictive models based on environmental (entry), colonization, establishment and covariates in the native range of a pest can spread (Mack et al., 2000; With, 2002; lead to erroneous estimates of fi nal extent, Hennessey, 2004; Lockwood et al., 2005; either due to genetic diff erences in the Hulme, 2006; Drake and Lodge, 2006). For invading population or due to diff erent brevity, we lump the fi rst three processes relationships between the pest and under the heading of colonization and then unidentifi ed covariates (Fitzpatrick et al., look at dispersal. In this simplifi ed 2007). It also needs to be recognized framework, colonization deals with the that the destination areas encompass internal processes within a defi ned area both spatial and temporal environmental while dispersal deals with the exchange of variation (Jarvis and Baker, 2001b; organisms between areas. Simberloff , 2009). In simplest terms, colonization is the Th e exposure of an area to the risk of process of a defi ned area going from pest introduction is commonly referred to uninfested to infested. As any infested area as propagule pressure (Leung et al., 2004; poses a biosecurity risk, estimating Lockwood et al., 2005; Carrasco et al., colonization events is fundamental to the 2010b). A propagule is a group of one or spatial management of invasive pests. Much more organisms that enters an area at a work has focused on colonization across particular time, while the propagule national borders (Drake and Lodge, 2006; pressure is the total exposure of an area to Holmes et al., 2009; Simberloff , 2009). Th e these over some period of time (Simberloff , 28 Megan Quinlan et al.

2009). Exposure assessments for environ- this eff ect (Kramer et al., 2009). In order to mental pollutants have used epidemiological defi ne the hierarchical link between risk characterization techniques at a observations and pest status, models of sophisticated level (Nieuwenhuijsen et al., colonization need to represent the 2006) but these are yet to be investigated population states within the area over time. rigorously with respect to colonization in Given that it is diffi cult to collect empirical invasions (Stohlgren and Schnase, 2006). Of information on the colonization phase, interest to biosecurity are estimates of the much of the burden for providing prior probability that an area is free of a pest at ecological knowledge falls upon dispersal some time. One approach is to implement models. discrete time models for the number of Invasive pests can spread by a number propagules arriving at a destination and of natural dispersal mechanisms, including surviving. Jerde and Lewis (2007) adopt a along drainage lines, wind-assisted fl ights Poisson model for the survivors as the sum (Reynolds and Reynolds, 2009) or active of movements from all pathways into the fl ight (Guichard et al., 2010). Additional destination and use a geometric distribution human-mediated dispersal pathways may to estimate the waiting time for a also exist on nursery stock (Smith et al., colonization event in discrete time. A similar 2007), produce (Areal et al., 2008) or simply approach was used by Leung et al. (2004). as incidental hitchhikers (Ward et al., 2006). Th e fate of organisms between entry Spatial connectivity processes for natural and establishment is one of the great dispersal and human-mediated dispersal unknowns of invasion biology (Puth and underpin biosecurity management problems Post, 2005), and is perhaps the most diffi cult (Diggle, 2006). process to parameterize. Early stages of the Several spatial frameworks have been colonization processes are poorly under- used to provide the scaff olding for modelling stood, most notably because they are rarely invasions and pest dispersal. On continuous observed and there is little empirical space and time, the classic deterministic evidence on processes that lead to reaction–diff usion models of Skellam establishment (Simberloff , 2009). A handful (1951), based on random movements of of studies have attempted to quantify the individuals, formed the basis of invasion number of propagules being moved along research for decades. Integro-diff erence pathways (Stanaway et al., 2001; McCullough equations (IDE) off er a discretized et al., 2006; Lee and Chown, 2009), however, methodology for implementing invasive these are diffi cult to relate to the dispersal with the fl exibility of diff erent establishment of populations in new areas. dispersal kernels (Neubert and Parker, Successful establishment is based upon 2004). Dispersal kernels model the the fates and reproductive success of what probability of movement between two areas is generally a small founding population as a function of Euclidean distance. While (Kawasaki et al., 2006). Th erefore, Gaussian kernels are commonly used (Havel stochasticity plays a central role in under- et al., 2002; Wikle and Hooten, 2006; standing and modelling the colonization Chapman et al., 2007), other distributions process. In particular, there is potential for used for dispersal kernels include Laplace initially low rates of population increase and (Lewis and Pacala, 2000; Neubert and spread, known as Allee eff ects, that can Caswell, 2000), Cauchy (Mayer and Atzeni, cause local extinction after the introduction 1993), exponential (Havel et al., 2002) and (Hastings, 1996; Foley, 2000; Keitt et al., negative exponential (Chapman et al., 2007). 2001; Dennis, 2002; Drake and Lodge, Dispersal kernels with exponentially 2006). While Allee eff ects may contribute bounded tails lead to asymptotically signifi cantly to the success and expression constant rates of spread through continuous of the colonization process, prohibitively space, while others, for example the Cauchy intensive collection of data from populations distribution, can lead to accelerating rates of at low densities may be needed to quantify spread (Kot et al., 2004). One of the Biosecurity Surveillance in Agriculture and Environment 29

drawbacks of IDEs is that they are evidence for the dispersal distances of deterministic and provide for a continuous individuals is diffi cult to collect but can be distribution of organisms rather than a used to estimate dispersal kernels (Kareiva, discrete distribution of individuals. 1983; Hawkes, 2009). Where long-distance Incorporating stochasticity on discrete movement is a prime contributor to individuals can slow the rate of spread (Kot invasions, uncertainty about rates of spread et al., 2004) so that even fat-tailed kernels can prohibit meaningful inference about can lead to asymptotic rates of spread (Clark distribution (Clark et al., 2003). et al., 2001, 2003). Plant biosecurity surveillance is de - While continuous space models can ployed and evaluated according to some have attractive mathematical properties, (generally informal) underlying mechanistic their application to heterogeneous environ- model of pest ecology (Plant Health ments can be problematic. As biosecurity Australia, 2010). While mechanistic models programmes frequently deal with spread may be formulated diff erently, the spatial through geographically fragmented host realization of these models may be similar landscapes, another option is to look at the (Wikle, 2003). What is more important for transfer rates of propagules between discrete managing high-priority plant pests is that areas. Connectivity models provide a more the model can be translated into operational tractable framework for working with use for the appropriate management units, discrete patches that may exchange whether they are countries, districts, farms, propagules (Urban and Keitt, 2001). Rates blocks within a farm, trees within a block or of exchange may again be modelled as a a continuous landscape of wild hosts. Pest function of distances to known infested spread across a landscape of plant host sites using the same dispersal kernels as for material requires critical examination as a continuous landscapes. Gravity models to spatial model (With, 2002). Whether it is for predict the colonization rates of lakes by early detection, incursion management or to zebra mussels have been one successful justify pest-free areas, these ecological application of this approach (Bossenbroek et models provide the dynamic context for al., 2001). Similar approaches on lattices interpreting surveillance data. that defi ne connectivity as bond strengths between neighbouring areas are commonly used in epidemiology (Sander et al., 2002; 2.6.4 Statistical models Dybiec et al., 2004, 2005; Otten et al., 2004; Shirley and Rushton, 2005; Gibson et al., Statistical approaches to inferring extent 2006; Zhou et al., 2006). As these models commonly rely on generalized linear models deal with the links between individual to relate species distribution to environ- ecological units of interest, they off er readily mental covariate data, however, such models interpretable statistics for the management ignore the intrinsic spatial correlation that of spread between areas (Urban and Keitt, is a feature of where individuals are found 2001; Shirley and Rushton, 2005). (Latimer et al., 2006; Wintle and Bardos, Incursions typically spread through 2006; Dormann, 2007a; Hoeting, 2009; adjacent areas at both fi ne and coarse scales Beale et al., 2010). Auto-models provide an (Scherm et al., 2006). Most invasive species extension to regression models to allow the arrive in countries due to the activity of spatial covariance between sites within a people and continue to travel on similar neighbourhood to be admitted to the human-mediated pathways after arrival as analysis (Besag, 1972, 1974). Th is auto- well as by natural dispersal. Invasion covariance term may be based on Gaussian, processes can be highly stochastic with the binomial or Bernoulli distributions. colonization of satellite sites outside of the In the broader class of auto-models, contiguously infested area, a major driver of conditional autoregressive (CAR) models the overall spread (Lewis and Pacala, 2000; have been increasingly used for disease Neubert and Caswell, 2000). Empirical mapping applications (Lawson, 2009), 30 Megan Quinlan et al.

particularly as the algorithms to implement To delimit pest extent in a Bayesian these models within Markov chain Monte model, inference on the pest status of each Carlo (MCMC) software are freely available area of interest from the surveillance data (Th omas et al., 2004). For the analysis of requires some underlying invasion process. presence/absence data, autologistic models Gibson et al. (2006) describe a percolation have become a mainstay of species model to estimate the disease infection distribution problems (Augustin et al., 1996; times of plants on a lattice by considering Huff er and Wu, 1998; Hoeting et al., 2000) the diff erence in colonization times between although their performance under con- neighbouring plants to be exponentially ditions of strong spatial association has distributed. A feature of biosecurity data is been questioned (Dormann, 2007b; Carl and that often thousands of spatially referenced Kuhn, 2007). It is uncertain over what range data points are collected but when detection of scenarios a predominantly spatial model probabilities are low, the information can implicitly incorporate the temporal available to distinguish parameters can lead processes of invasions. Spatio-temporal to poor convergence properties for highly extensions to the autologistic model have parameterized models (Webster et al., 2008). been applied to pest outbreaks under the Furthermore, incorporating the space–time assumption that the spatial and temporal information contained in these points into components of the autocovariance are MCMC models becomes computationally separable (Zhu et al., 2008). As dynamic prohibitive. Banerjee et al. (2008) and processes in space and time may not be Latimer et al. (2009) propose predictive separable, explicitly modelled space–time process models that may overcome some processes must be developed for greater computational hurdles by modelling power of inference and interpretation of invasion processes at a manageable number management strategies (Wikle and Royle, of points in space and time. 1999). One of the main limitations of spatio- Th e dimensional complexity of space– temporal auto-models for biosecurity time models makes evaluation com- applications is their inability to accommodate putationally intensive and requires research the dynamic nature of a pest invasion as it to determine workable incursion manage- unfolds. ment scenarios. Some level of spatial and Wikle (2003) introduced reaction– temporal model aggregation is required to diff usion equations for pest spread and partition the system into computationally reproduction into a hierarchical Bayesian (operationally) manageable components for framework to estimate arrival times of which conditional probabilities of absence invading house fi nches. Th is and related can be determined. studies (Wikle and Hooten, 2006; Hooten et Quantitative analysis of biosecurity al., 2007; Hooten and Wikle, 2008), used surveillance data faces some signifi cant integro-diff erence equations with spatially hurdles for interpreting the distribution of varying diff usion coeffi cients to structure invading species. Ecological complexity the spatial transition of populations in must be captured by process model such discrete time steps. As the parameter of that they adequately portray uncertainty interest was the spatially varying rate of over space and time. On the other hand, spread, these authors specifi ed a log- assimilation of information from large data normally distributed population process, sets into high-dimensional models also but with the population set to zero according imposes computational challenges for to some reasonable boundary conditions. estimating extent and other parameters. While the hierarchical Bayesian modelling Biosecurity managers need to make pest framework they developed marked a major management decisions based on information advance in the analysis of invasion data, from expert ecological opinion and from further extension of their models is required large spatio-temporal surveillance data sets. to focus the inference on the estimation of Moreover, decisions are often required pest boundaries. urgently in the face of uncertainty. Th e Biosecurity Surveillance in Agriculture and Environment 31

adoption of quantitative techniques will obtained, in the surveillance study. Th is only occur when they directly support the needs to take into account the survey and management aims of biosecurity agencies sampling design, the population char- within their operational decision-making acteristics of the pest, its potential pattern environments. of incursion, the probability of missing the pest if it is present, and so on. Since the observation model can only provide evidence 2.7 Discussion about presence at a particular population density, it must in turn be complemented by We opened this chapter with a discussion of a spread or invasion model that describes two issues that impact on the future of the pest’s likely spatial and temporal biosecurity surveillance: (i) the defi nition of intensity. the term itself; and (ii) the activities that the Th ese geographic models, observation term encompasses. models and invasion models are themselves As indicated in the Introduction, the comprised of sub-models that describe defi nitions of biosecurity, and even of important components of the problem. For biosecurity surveillance, are quite broad and example, an observation model requires the scope of these terms is evolving and sub-models for pest detectability and for expanding. While plant and animal health the status of the pest over space and time. practitioners relate well to the term as Similarly, an invasion model requires familiar within their respective frameworks, sub-models that describe the spatial they may drop the ‘plant and animal’ preface process of pest dispersal, which may include when discussing biosecurity, thereby one or more deterministic reaction– recognizing it as diff erent from simply a diff usion rep re sentations, continuous combination of the previously existing two space–time repre sentations, connectivity or sectors. Biosecurity-related decision making gravity represent ations, or fully Bayesian depends critically on reliable evidence. A key stochastic representations. Th ese sub- source of such evidence is through models require careful choices of parameters surveillance. Th is requires not only careful and associated statistical distributions, design and implementation of surveillance which in turn inform the statistical analysis schemes, but also appropriate statistical of the surveillance data. For example, the modelling and analysis of the surveillance sub-model of pest detectability determines outputs. Th is chapter has presented an the manner in which overdispersion is dealt overview of these approaches. Most of them with in the resultant data, while space–time are focused on the evaluation of risk, that is, correlations will determine the method for the synthesis of the probabilities and temporal discounting of the surveillance consequences of pest entry, establishment data. and spread. Not only must decisions be made about Eff ective analysis of surveillance data the form of the geographic, observation and requires careful attention to the development invasion models and sub-models, but the of appropriate statistical models at both the statistical representations of the model design and the analysis stages of the components must also be carefully surveillance activity. At the design stage, a considered. A number of relevant statistical geographic model can describe the spatial models have been described in this chapter, and temporal scales and units required for including generalized linear models and decision making, data collection and spatial autoregressive models to infer extent, ecological modelling, as well as the potential reaction–diff usion and diff erence equations area of pest risk, the hosts and pathways of for pest spread and reproduction, and the pest, and other key considerations. Th e percolation models to infer pest status at an geographic model must be complemented by area of interest. Th ese models can be cast in an observation model that describes the deterministic, frequentist or Bayesian stoch- presence/absence data obtained, or to be astic frameworks, or a combination of both. 32 Megan Quinlan et al.

Th e geographic, observation and organizations with respect to the particular invasion models are not independent. defi nitions of biosecurity surveillance and Components of one model are necessarily the corresponding activities undertaken linked to components in the other models. under its auspices. Th is is natural given the For example, the sub-model that describes diff erent focal areas of these organizations space–time correlations in the geographic and the environments in which they operate. model is strongly linked to the description However, as illustrated in this chapter, it has of the dynamic processes of pest spread of the potential to induce confusion and space and time required in the invasion misalignment among stakeholders. Th is process model. Similarly, the geographic chapter thus serves the purpose of providing model will inform the component processes both a review and a clarifi cation of bio- of entry, colonization, establishment and security surveillance, to assist in creating a spread considered in the invasion model, as more consistent understanding of this fi eld. well as the habitat suitability sub-models Th is shared understanding of the that underpin these processes. Th e spatial defi nition of biosecurity surveillance leads and temporal scales determined in the naturally to an agreed understanding of the surveillance design phase impacts on all of activities that it encompasses. Th is depends the models and the resultant analyses. on a combination of intrinsic and extrinsic Th ere are many diffi culties in con- factors. Intrinsic factors include the structing and employing these types of organizational and operational aspects of surveillance models. Th ese include: (i) the biosecurity surveillance itself. Maintaining availability of required information in a fl exibility and longevity in biosecurity sur- timely manner; (ii) the decision making veillance programmes is a constant balancing required to decide on the appropriate act, since both are essential to eff ective biological and statistical descriptions of the surveillance. Moreover, sharing of infor- model components and processes; (iii) the mation, including data and results, across computational imple ment ation of the organizations and programmes will become statistical analyses; and (iv) the practical an increasingly important feature of future interpretation of the analytic results. It is surveillance, particularly in light of important that these diffi culties are seen as globalization, climate change and new data an opportunity for improvement of the sources. Th ese extrinsic factors also include methods and tools used for biosecurity, population growth and trends, industrial- rather than as an unassailable obstacle ization and new pathways such as the in evidence-based biosecurity decision internet. Th ese will all infl uence how bio- making. Moreover, the development of security surveillance is conducted in the these models can be viewed as an avenue for future. creating closer links between the various Importantly, a key extrinsic factor is the sectors and corresponding organizations placement of biosecurity surveillance in the involved in biosecurity. It is hoped that the broader biosecurity regime. For example, we summary provided in this chapter, along have found that biosecurity goes much with the statistical issues and methods farther than the combination of animal and described in other chapters of this book, plant health, to provide more holistic motivates further consideration and uptake coverage of biological threats, addressing of these approaches, as appropriate. naturally occurring, and accidental and In this chapter we have reviewed the intentional man-made threats to bio- various defi nitions and characteristics of diversity, health, food and even public safety. biosecurity surveillance and its place in the It is therefore important to identify the broader picture of plant and animal role that surveillance plays in the context biosecurity. It is evident that while the of the other dimensions of this broader general intent of biosecurity surveillance is regime, in order to appreciate its value, consistent, there are diff erences among optimize resources and improve outputs and international, national and regional outcomes. Biosecurity Surveillance in Agriculture and Environment 33

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9781780641645.pdf

ISBN: 9781780641645 Contents

Contributors vii Foreword xi 1 Introduction 1 Jeff rey S. Dukes and Lewis H. Ziska

Part I - The Dimensions of the Problem: Background and Science 2 Communicating the Dynamic Complexities of Climate and Ecology: Species Invasion and Resource Changes 9 John Peter Th ompson and Lewis H. Ziska 3 Climate Change and Plant Pathogen Invasions 22 Karen A. Garrett, Sara Th omas-Sharma, Greg A. Forbes and John Hernandez Nopsa 4 Analysis of Invasive Insects: Links to Climate Change 45 Andrew Paul Gutierrez and Luigi Ponti 5 Climate Change, Plant Traits and Invasion in Natural and Agricultural Ecosystems 62 Dana M. Blumenthal and Julie A. Kray

Part II - Case Studies 6 Non-native Species in Antarctic Terrestrial Environments: Th e Impacts of Climate Change and Human Activity 81 Kevin A. Hughes and Peter Convey 7 Synergies between Climate Change and Species Invasions: Evidence from Marine Systems 101 Cascade J.B. Sorte 8 Ragweed in Eastern Europe 117 László Makra, István Matyasovszky and Áron József Deák 9 Climate Change and Alien Species in South Africa 129 Ulrike M. Irlich, David M. Richardson, Sarah J. Davies and Steven L. Chown

v vi Contents

10 Climate Change and ‘Alien Species in National Parks’: Revisited 148 Th omas J. Stohlgren, Jessica R. Resnik and Glenn E. Plumb 11 Invasive Plants in a Rapidly Changing Climate: An Australian Perspective 169 Bruce L. Webber, Rieks D. van Klinken and John K. Scott 12 Invasive Species of China and Th eir Responses to Climate Change 198 Bo Li, Shujuan Wei, Hui Li, Qiang Yang and Meng Lu

Part III - Management: Detection and Prevention 13 Identifying Invasive Species in Real Time: Early Detection and Distribution Mapping System (EDDMapS) and Other Mapping Tools 219 Rebekah D. Wallace and Charles T. Bargeron 14 Global Identifi cation of Invasive Species: Th e CABI Invasive Species Compendium as a Resource 232 Hilda Diaz-Soltero and Peter R. Scott 15 Th e Biogeography of Invasive Plants – Projecting Range Shifts with Climate Change 240 Bethany A. Bradley 16 Identifying Climate Change as a Factor in the Establishment and Persistence of Invasive Weeds in Agricultural Crops 253 Antonio DiTommaso, Qin Zhong and David R. Clements 17 Assessing and Managing the Impact of Climate Change on Invasive Species: Th e PBDM Approach 271 Andrew Paul Gutierrez and Luigi Ponti

Part IV - Management: Control and Adaptation

18 Climate, CO2 and Invasive Weed Management 293 Lewis H. Ziska 19 Early Detection and Rapid Response: A Cost-eff ective Strategy for Minimizing the Establishment and Spread of New and Emerging Invasive Plants by Global Trade, Travel and Climate Change 305 Randy G. Westbrooks, Steven T. Manning and John D. Waugh 20 Adapting to Invasions in a Changing World: Invasive Species as an Economic Resource 326 Matthew A. Barnes, Andrew M. Deines, Rachel M. Gentile and Laura E. Grieneisen Index 345 Global Identiﬁ cation of Invasive Species: The CABI Invasive 14 Species Compendium as a Resource

Hilda Diaz-Soltero1 and Peter R. Scott2

1USDA, Ofﬁ ce of the Secretary, Washington, DC, USA; 2CAB International, Wallingford, UK

Abstract Introduction

Th e number, spread and impact of invasive As climate change and rising CO2 levels species in the latter half of the 20th century impose additional risks regarding the has been without historical precedent. Now, introduction and spread of invasive species as human activity causes a precipitous rise (Mooney and Hobbs, 2000), new and in greenhouse gas emissions (e.g. CO2), eff ective management methods are needed. there is growing concern that climate change Chief among these is the strategy of may also be a signifi cant, long-term driver detection and prevention, i.e. to keep track enhancing invasive species introduction and of invasives through visual recognition and spread. New and more powerful tools that assess their potential for environmental or facilitate linking invasive species and climate economic harm. Th e introduction and change are required to identify and manage demography of invasive species is tied to these consequences. One such tool, which global trade (Hulme, 2009), with con- exploits a wide range of traditional and sequences for ecology and agriculture social media, is the Invasive Species (Pimentel et al., 2005; Ziska et al., 2011). To Compendium, or ISC. Th e ISC is a scientifi c, manage invasive species, a comprehensive web-based encyclopedia that compiles the means to identify, track and, if possible, latest information on the invasive species eliminate them is needed. It is from this that have the most negative impacts on the perspective that the global Invasive Species environment, the economy and/or animal or Compendium (ISC) was developed. Pre- human health. Th e information in the ISC, viously, knowledge about a given invasive updated weekly with the latest scientifi c species was often sporadic, specifi c to a fi ndings, can be used; to infer future climate given region, and not integrated spatially or change impacts on an invasive species; to temporally. Increasing international trade, understand the potential environmental in combination with changes in climate, and/or economic impacts of the species, and lend urgency to the need for an integrated, to identify ways to control and manage the publically accessible, continuously updated species in question. Th is chapter discusses invasive species resource at no cost to the the value and effi cacy of the ISC, with a user. Such a resource may be especially particular emphasis on its application in a relevant to developing countries that may globally warmed future. lack technical information on invasive

232 © CAB International 2014. Invasive Species and Global Climate Change (eds L.H. Ziska and J.S. Dukes) The Invasive Species Compendium as a Resource 233

species management or in countries/regions Th e impacts of these organisms on where trade and climate are undergoing natural ecosystems and on biodiversity are rapid changes. To develop such a resource, considered, as well as their impacts on the global ISC was initiated as a means to systems managed for agriculture, agro- provide scientifi c information on invasive forestry, aquaculture and animal health. species that was widely accessible, region Economic impacts are documented, as well specifi c and temporally accurate. as potential adaptive uses (see Chapter 20, this volume). While an underlying goal is to ingrate global knowledge, a geographic The Invasive Species Compendium: information system (GIS) is also used to An Overview display distributions of invasive species at the country, state and province levels. Th e Th e ISC is a multimedia encyclopedia that ISC also includes information the invasive includes information regarding several species’ pathways and vectors, as well as thousand invasive species (available at available methods regarding control and http://www.cabi.org/isc/). Th e ISC is, at management. Extensive reference materials present, the most extensive and author- are included, including images, library itative compilation on all taxa of invasive documents (including peer-reviewed journal species. It includes, globally, known invasive articles), conference papers and reports, organisms across all ecosystems – aquatic, bibliographic abstracts and a glossary of marine or terrestrial – that cause the most technical terms, as well as comprehensive harm. Since its release in 2012, the tool has links to relevant identifi cation keys and been updated weekly and is available on an image libraries. As of June 2013, there were open-access basis. over 1682 full invasive species data sheets Th e ISC was developed by a consortium of and over 7291 abbreviated data sheets in organizations from 12 countries that the ISC. contributed fi nancially to its development. Th e eff ort to develop the ISC was led by CAB International (CABI) in association with the Data Sources for the ISC US Department of Agriculture (USDA). Th ey are partnered by expert organizations Th e content for the ISC data sheets is derived including the European and Mediterranean globally from thousands of expert scientists. Plant Protection Organization (EPPO) and Th e ISC’s veracity derives from their the World Organisation for Animal Health expertise, from corroboration through peer (OIE). CABI, an international, non-profi t, review and through rigorous editing for science-based, knowledge organization, has quality control. a mission to provide information and apply Additional content is derived from scientifi c expertise to solve problems in existing compilations of knowledge on agriculture and the environment (CABI, invasive species, including expert organ- 2012). izations such as the Inter-American Th e objective of the ISC eff ort was to Biodiversity Information Network, the provide an international resource with currently inactive Global Invasive Species respect to invasive species. In that regard, Programme and the Smithsonian National the ISC covers the identifi cation, biology, Museum of Natural History. Content is distribution, impact and management of presented dynamically in the ISC through an thousands of invasive species. Invasive advanced web-based platform combining species of all taxa are covered, including databases, text and images. GIS, taxonomic plants, fungi, bacteria, viruses and animals. relationships and data suitable for decision- Subcategories of animals are further dis- support tools, such as risk analysis data, are tinguished into insects, nematodes, molluscs also provided by the ISC in an interactive and vertebrates. framework. 234 H. Diaz-Soltero and P.R. Scott

Any user accessing the ISC can also link to resources. Th e Consortium’s goal is to provide information both within the ISC and with a ubiquitous resource that: (i) is easily acces- other local or remote knowledge bases. Th e sed; (ii) is relevant at diff erent biogeographical content is updated weekly, and the ISC will scales; (iii) is biologically accurate; and (iv) be maintained, enhanced and updated provides control and management options regularly into the foreseeable future. for invasive species. Because such a resource must be temporally relevant, the ISC continues to be updated regularly as new Management and Financing of information becomes available. the ISC A primary goal of the ISC is accessibility. It should be widely available to an extensive Th e ISC Consortium, a group of supporting group of stakeholders. To make the ISC free organizations (Table 14.1), provides the to its users, development costs are shared strategic direction and scientifi c leadership among Consortium Members. At present, for the ISC project, as well as fi nancial the budget for the development and

Table 14.1. Consortium members of the Invasive Species Compendium. Australia, Group Membership Cooperative Research Centre for National Plant Biodiversity, CRCNPB Grains Research and Development Corporation, GRDC Horticulture Australia Limited, HAL Invasive Animals Cooperative Research Centre, IACRC Australian Centre for International Agricultural Research (ACIAR) Canadian Food Inspection Agency; Forest Service; and International Development Agency Caribbean Island Countries (sponsored by European Union DGDEV) France, Ministry of the Environment Forum for Agricultural Research in Africa (sponsored by DFID) India, Ministry of Agriculture Malaysian Agricultural Research and Development Institute Mexico National Health, Safety and Quality Service for Agri-Food, SENASICA Comisión Nacional para el Conocimiento y Uso de la Biodiversidad, CONABIO Monsanto Corporation Netherlands Ministry of Economic Affairs, Agriculture and Innovation Secretariat of the Paciﬁ c Community (SPC) Swiss Agency for Development and Cooperation Syngenta Crop Protection UK Department for Environment Food and Rural Affairs, DEFRA Department for International Development (DFID)/CABI/FARA US Agency for International Development (USAID) US Department of Agriculture: Agricultural Research Service (ARS); Animal and Plant Health Inspection Service (APHIS); Foreign Agricultural Service (FAS); Forest Service (USFS); Invasive Species Coordination Program; Natural Resources Conservation Service (NRCS); Rural Development (RD) US Department of Commerce, NOAA’s National Ocean Service (NOS) US Department of the Interior, U.S. Fish and Wildlife Service (FWS)

Note: New Members are expected from Latin America, Asia, Australasia, Europe and North America. Any country, non- governmental organization, private company or industry can become a member; most members are in the environment or agriculture arena, and work on invasive species issues. Participation is voluntary and by invitation. The Invasive Species Compendium as a Resource 235

maintenance of the ISC is US$4.75 million development, ongoing maintenance and over an 8-year period until 2016. enhancement. Membership presents a Contributions from more than 29 Members visible token of participation and leadership of the Development Consortium, based in a project that is positioned to reduce the in 12 countries, have amounted to more economic and environmental impact of than US$4.75 million to date. Of this, invasive species globally. Members have an US$3 million covered the phase of develop- opportunity to discuss and infl uence ment and release of the defi nitive ISC. Th e common interests in an international forum remaining US$1.75 million covers the task of like-minded representatives of public and of updating, maintenance and enhancement. private sector organizations and develop- Additional funds are sought continuously, to ment assistance agencies. include emerging invasive species and to enhance the current information base. Such funds are also critical in extending the Development of the ISC period of updating, maintenance and enhancement beyond 2016. Th e development of the ISC has taken place New Consortium Members are asked in phases. Th e fi rst phase was completed to make a one-time contribution of after 18 months in 2008 and delivered an US$175,000 (US$130,000 for developing alpha version covering work to document country organizations), paid over 1 or 2 1000 invasive species. Th is was made years. Each new Member makes an essential available to the development Consortium contribution towards the development Members for use and feedback. During the target. No distinction is made regarding second phase, information on 500 more when a member joins the Consortium. species was added, with enhanced develop- Organizations that join the Consortium ment of the IT platform and with the benefi t in several ways. Participants have development of advanced search tools. Th e the opportunity to leverage the contributions beta version, with extended content and of all the other Members and to receive the enhanced functionality, was released in benefi ts of a multi-million dollar develop- October 2010. A revised beta version was ment based on global expertise. Membership released to the public in June 2011, with the allows participants to ensure that their own fi nal, defi nitive version in April of 2012 (see priorities are duly considered in the ISC’s Table 14.2; CABI, 2012).

Table 14.2. Features of the Invasive Species Compendium. The April 2012 version of the ISC includes: Fu ll data sheets on more than 1500 invasive species and related topics prepared by 1000 specialists from throughout the world, peer-reviewed and edited by CABI. A single data sheet for an invasive species includes: Identity: including names, taxonomy, description Images Distribution: including global and regional maps Biology and Ecology: including habitat, host species, genetics, physiology, environmental requirements, epidemiology, vectors, natural enemies Impact: including economic, environmental, cultural Management: including diagnosis, detection and control (regulatory, genetic, cultural, chemical, biological) Gaps in knowledge/research needs References: linked to abstracts and, where available, to full text Additional data sheets on a further 7000 species 4000 images More than 75,000 abstracts of the published literature on invasive species (added to weekly) Full text of more than 1085 relevant published documents (added to weekly) Powerful search and browse facilities 236 H. Diaz-Soltero and P.R. Scott

Th e third phase of the ISC relates to security (through the productive use of land sustainability. Specifi cally, the ISC will be and water) and concurrent impacts on the updated continually, both in regard to environment and biodiversity. information and also to accessibility and Th e ISC has intrinsic value for preventing use. Th is process will involve the input and the introduction of invasive species participation of Consortium Members, as (including providing data for tools with well as feedback from users. At present, the predictive capability) by providing timely business plan covers these additional costs access to information on potential intro- until 2016, with the intention of indefi nite ductory pathways, as well as the management continuation. and containment of established invasive How can the ISC be improved for the species. In addition, it has utility in future? Proposed actions for Stage 4 of the extension, training, public awareness and ISC include: better GIS tools for assessing the research and development, and may provide impact of climate change on invasive species a scientifi c tool for policy decisions. Th e ISC biology; training people to use the ISC; is especially valuable in the local production linking population decline or the extinction of educational materials – for example, of native, threatened species to specifi c public information notices and training invasive species and documenting it in the techniques specifi c for a given bio- ISC; expanding information on biological geographical region. All information, text mechanisms that enhance invasive species and photographs in the ISC can be down- establishment; developing new scientifi c loaded to prepare educational materials tools for extinction vulnerability (population specifi c to local needs. and habitat viability analysis and meta- model analysis); establishing and extending the capacity of the ISC to communicate and Application of the ISC for exchange data with national invasive species the Detection and Prevention of databanks/inventories; enhancing/updating Invasive Species with Climate information on the biological control of Change invasives (updated global database on biological control); and augmenting the Anthropogenic increases in atmospheric number of invasive species with full data carbon dioxide, and the resultant increases sheets. in climatic variation, are among the most challenging issues in global biology (IPCC, 2007). Use and Access Th ese changes have a number of implications for the biology of invasive Open access, free at the point of use, was species. For example, increased carbon proposed and agreed at the ISC Inception dioxide could favour weedy invasive species Workshop in 2006. Th e costs of ISC such as cheatgrass, exacerbating the environ- maintenance are covered by the ISC mental damage from large, cheatgrass- Consortium contributions. fuelled fi res in some regions (Ziska et al., Th e ISC is freely available for use as a 2005). Although additional data are needed, global knowledge base to address practical initial studies have suggested that, on issues concerning the impact of thousands average, invasive species may show a of invasive species – on the environment, on stronger response to both recent and biodiversity and on agriculture, forestry and projected changes in carbon dioxide relative fi sheries, and on animal health. In June to native plant species (Song et al., 2009). 2012, the Compendium content was licensed Climate change, particularly warmer under a Creative Commons Attribution- temperatures, could also result in shifts NonCommercial-NoDerivs 2.0 UK: England of invasive species’ ranges, sometimes and Wales Licence. It spans the boundary leading to net expansions or contractions between invasive species’ impacts on food (Parmesan, 1996; Bradley et al., 2009). The Invasive Species Compendium as a Resource 237

Clearly, there is a need to have tools that countries; or, alternatively, from countries can assist in predicting the behaviour of with similar climate and/or soils. Cross- invasive species under diff erent climate comparisons can be made in order to change scenarios. Th e ISC can provide a fi rst elucidate new threats or to assess the assessment. Here are some examples on how economic or environmental vulnerability of the ISC can be used for purposes related to a given country or region to proximate climate change. invasive species. Th e ISC can then provide a list of invasive species that may present a risk. Th e GIS capability of the ISC can be Assessing the future range of an invasive used to do this task. As a result, any country species can prepare prevention actions and early detection and rapid response (EDRR) Th e ISC contains information on the programmes as management tools to cope preferred climate for a species: temperature, with new invasive threats. rainfall, soils (of a plant species), etc. Th ese Th is assessment can be a two-step data are contained in tables in the Biology process. Th e ISC search capability can be and Ecology section of the ISC’s Invasive deployed to compile a list of invasive species Species data sheets. Th e optimal climate in country X that are not in country Y at data relative to optimal growth and present. Extrapolating the ISC data using fecundity of an invasive species can be the ISC search capability can be used with exported via text or table formats, enabling other resources such as WorldClim (www. them to be used for specifi c and sophisticated worldclim.org) climate projection models to climate models. Th e ISC can also export investigate the invasive species of a country distribution data to a Google map using a (country X) with a climate that is the same KML (Keyhole Markup Language; a map fi le as or similar to that predicted for another format that can display distribution data) country (Y) some time in the future. Th ose download tool. Layering freely available species identifi ed as present in X but not in Y present-day climate data under the could then be prioritized in national invasive distribution of a species could be used to species prevention and management pro- explore, using maximum entropy or other grammes in country Y; programmes which techniques, the range change of the species could also be informed by other data in the predicted by future-climate-change models. ISC such as those relating to known pathways of introduction. What are the invasives in my country?

Th e ISC can make a list of the invasive Analysing pathways for invasive species’ species present (those that have a full data introductions with climate change sheet) for any country. For some countries, the information can be obtained at the state Th e ISC will have a data sheet for over 50 or province level. Th is can serve as a starting pathways used by invasive species. For a point for land managers, scientists and particular proposed climate change scenario, others to examine the regional threats posed pathways that might be used by an invasive by invasive species for their area. Such an species to enter a country can be identifi ed, assessment may also identify adjoining and as a result, management strategies to invasives that could potentially migrate in mitigate or prevent introductions can be response to climate change (McDonald et al., developed and implemented. 2009). Analysing invasive species by habitat Assessing the threat of new invasives under climate change

A list of known invasive species can be In the near future, over 45 habitat data requested from other geographically close sheets will be included in the ISC, providing 238 H. Diaz-Soltero and P.R. Scott

lists of associated invasive species and database of current and potential threats, collating information on the specifi c risks, associated movements and biological and threats and management challenges in - ecological characteristics, will provide a vasive species pose to each of those habitats. freely available, unique, easily accessible, Th e name of the habitats in the ISC is worldwide resource to assist with the contained in the ‘Advanced Search Help’. detection and management of invasive Some of the habitats included are agricultural species on a global basis. lands, forests, grasslands, roadsides, man- groves, salt marshes, lakes, streams, coral reefs, etc. For example, if we are interested Acknowledgements in knowing the invasive species that are found in the habitat called ‘terrestrial- Th e authors acknowledge the collaboration managed, forests’, we can query the ISC to and information on the ISC provided by list those invasive species associated with Lucinda Charles, Gareth Richards and such a habitat. Elizabeth Dodsworth of CABI. If there is particular concern about the range expansion of an invasive species References habitat under climate change, the ISC can also help. In our example, we might wish to Bradley, B.A., Wilcove, D.S. and Oppenheimer, M. pursue how invasive species within the (2009) Climate change and plant invasions: habitat, ‘terrestrial-managed, forests’, might restoration opportunities ahead? Global be impacted for a given IPCC scenario. Th e Change Biology 15, 1511–1521. ISC can be queried for a list of invasives in CABI (2012) Invasive Species Compendium. CAB that specifi c habitat throughout the world. International, Wallingford, UK (http://www.cabi. Th e list can then be refi ned by the specifi c org/isc/, accessed 27 January 2014). climate parameters (e.g. change in minimum Hulme, P.E. (2009) Trade, transport and trouble: temperature) that are projected for the managing invasive species pathways in an era of globalization. Journal of Applied Ecology 46, climate model in question. Identifi cation of 10–18. the invasive species associated with that IPCC (Intergovernmental Panel on Climate habitat will also generate a list of species in Change) (2007) Climate Change 2007: Impacts, neighbouring countries or regions with Adaptation and Vulnerability. IPCC Secretariat, strong trade links. Th at way, in conjunction Geneva, Switzerland. with other techniques described above, an McDonald, A., Riha, S., DiTommaso, A. and estimated list of all of the potential invaders DeGaetano, A. (2009) Climate change and the within that habitat and the range that geography of weed damage: analysis of US habitat might occupy between regions or maize systems suggests the potential for countries, can be examined. signiﬁ cant range transformations. Agriculture, Ecosystems and Environment 130, 131–140. Mooney, H.A. and Hobbs, R.J. (2000) Invasive Species in a Changing World. Island Press, Summary Washington, DC, 457 pp. Parmesan, C. (1996) Climate and species range. Anthropogenic carbon dioxide and associ- Nature 382, 765–766. ated changes in global climate will infl uence Pimentel, D., Zuniga, R. and Morrison, D. (2005) the distribution and biology of invasive Update on the environmental and economic species. Given the economic and environ- costs associated with alien-invasive species in mental damage infl icted by invasives, it is the United States. Ecological Economics 52, imperative that management tools that can 273–288. Song, L., Wu, J., Li, C., Li, F., Peng, S. and Chen, B. track, discern and help to prevent the (2009) Different responses of invasive and establishment of invasive species become a native species to elevated CO2 concentration. global priority. In this regard, the Invasive Acta Oecologia 35, 128–133. Species Compendium (ISC), by initiating Ziska, L.H., Reeves, J.B. III and Blank, R. (2005) and maintaining a comprehensive scientifi c The impact of recent increases in atmospheric The Invasive Species Compendium as a Resource 239

CO2 on biomass production and vegetative Ziska, L.H., Blumenthal, D.M., Runion, G.B., Hunt, retention of cheatgrass (Bromus tectorum): E.R. Jr and Diaz-Soltero, H. (2011) Invasive implications for ﬁ re disturbance. Global Change species and climate change: an agronomic Biology 11, 1325–1332. perspective. Climatic Change 105, 13–42. This chapter is from the book:

Climate Change Impact and Adaptation in Agricultural Systems

Author(s): Fuhrer, J., Gregory, P.J. Published by: CABI ISBN: 9781780642895 Climate Projections for 2050 1 Markku Rummukainen Centre for Environmental and Climate Research, Lund University, Sweden

1.1 Introduction expect its past behaviour to also give us a good picture of things to come, future In order to assess the implications of climate conditions are innately unknown to us. Th is change in terms of impacts and adaptation is especially true for the consequences of needs, projections of the future climate are the use of fossil fuels and land-use change, needed. Climate models are the primary which in creasingly adds greenhouse gases means of such simulations. Th e results are to the atmosphere, not least carbon dioxide often coined ‘climate scenarios’ but should but also methane, nitrous oxide, etc. Th ere really be called projections, as they are built are emissions that aff ect the tropospheric on alternative scenarios of future land-use ozone, which has an eff ect on the climate, changes and greenhouse gas emissions. Th e in addition to impacts on health and basis for climate projections is discussed in vegetation. Human activities also aff ect the this chapter, together with a selection of amount of sulfate particles and soot in the general results that are of key relevance for atmosphere, which further compounds our agriculture, which stem from state-of-the- impact on the climate. Land-use change, in art climate projections. Th is chapter provides addition to aff ecting carbon sources and the background for the subsequent chapters sinks, aff ects the physical properties of the in this book, and discusses climate pro- land surface, which further adds to the jections for the next few decades. While the forces that the climate now responds to on focus is on the period until 2050, it should global, regional and local scales (Pitman be noted that climate change will very likely et al., 2011). continue well beyond the middle of the 21st Th at we force the climate and that the century. Indeed, the long-term prospects are climate responds is certain (IPCC, 2007). about not only a changed climate but also a Climate change projections for the future climate that is changing over time, i.e. it is have, however, uncertainties. Th is should about con tinuous change over a long time. not be confused with the view that they are Th e same is thus also true for our knowledge left wanting; evaluation of climate models requirements regarding climate change suggests that they perform well in many impacts, as well as the motivation and need respects, and as they are based on physical for climate change adaptation; however, principles, their results do have considerable these may take form. credibility. Model shortcomings are one source of uncertainty. Scenario uncertainty con- 1.2 Basis for Climate Change cerning underlying future emissions and Projections land-use pathways is another. In addition, the climate system exhibits internal 1.2.1 General variability that arises from the complex interplay between the atmosphere, the While we observe and experience our ocean and the other climate system com- contemporary climate and intrinsically may ponents. Th e relative importance of these

sources of uncertainty is well established more versatile ones. Over the past 10 years (e.g. Hawkins and Sutton, 2009). or so, most global and regional climate pro- Climate projection uncertainty is smaller jections have been based on the IPCC Special at the global scale compared to the regional Report on Emissions Scenarios (SRES; scale – and even more so, compared to Nakićenović and Swart, 2000), which span a the local scale. Th is is due largely to the range of possible future emissions pathways. ubiquitous internal variability that can Th e most recent climate projections are simultaneously aff ect diff erent regions in based on the RCP scenarios (representative contrasting ways but which is largely concentration pathway; Moss et al., 2010). cancelled out in the global mean. Th e relative Th ese are coined RCP2.6, RCP4.5, RCP6.0 importance of internal variability for climate and RCP8.5. Th e SRES and the RCP scenarios projection uncertainty declines over time, as are set up in diff erent ways. Th e former the forced climate change signals become provides greenhouse gas emission and greater. At the same time, the uncertainty land-use change pathways, based on under- linked to the emissions and land-use change lying assumptions regarding socio-economic scenarios grows. Th e uncertainty attributed drivers such as population and economic to climate models has a more constant and technical development. Th e atmospheric presence compared to the other two factors. concentrations of greenhouse gases are then Th ese sources of uncertainty are discussed derived from the emissions scenarios, for below. use in climate models. Th e RCP scenarios provide radiative forcing/greenhouse gas concentration scenarios for the 21st century. 1.2.2 Climate-forcing scenarios: fossil Th e number attached to each scenario fuels and land-use change designates the radiative forcing in W m–2 by 2100. Th ere is an accompanying eff ort with Underlying climate model projections, i.e. RCPs for the generation of corresponding forward-looking simulations of the evolution greenhouse gas emissions, land use and of the climate system, are scenarios of socio-economic developments. climate-forcing factors. In terms of the Th ere is no one-to-one comparability of climate over the next few decades and the RCPs and the SRES, but they span much beyond, this concerns anthropogenic emis- of the same range of alternative future sions of greenhouse gases, particles and their climate forcing. Th e RCPs, however, also precursors and the indirect greenhouse gases include a scenario (RCP2.6) that corresponds (see above), as well as land-use change. While to considerably lower emissions than any of today’s energy systems, consumption pat- the SRES scenarios, and as such is aligned terns, food and fi bre production do lock us with a considerable mitigation eff ort. Still, on to a path of continued climate change in neither the SRES nor the RCPs are recom- the short and medium term, the longer-term mendations for policy, or forecasts. Th ere situation is less certain. Th us, scenario are no probabilities affi xed to them. assumptions of emissions and land-use Overall, when interpreting climate model change are an important part of uncertainty results, information is needed about the in climate projections. underlying emissions and land-use scenarios, Knowledge of both the underlying as climate change projections largely scale climate-forcing scenario (emissions, land- with the emissions scenario. How much so use change) and of the climate model (cf. depends, however, on the climate models ‘climate sensitivity’, see below) is paramount themselves. when considering a specifi c climate change projection; for example, in terms of temperature change. Climate models, emis sions 1.2.3 Climate sensitivity and land-use scenarios have evolved over time. Early on, more or less idealized Alongside assumptions regarding the emis- scenarios were used, which were followed by sions pathways and future land-use change, a Climate Projections for 2050 9

second key uncertainty in climate change climate system to forcing. Solving the projections is the sensitivity of the climate equations in climate models requires, how- system. Simply put, this is a measure of how ever, extensive computational power, not much the climate changes when it is forced.1 least as simulations span from decades to Climate sensitivity is the net measure of the centuries and often need to be repeated with direct eff ect of the forcing and the feedback several variations. Th is constrains the that arises within the climate system. An resolution of the models. Even today, many example of key feedback is that a warmer global climate models have a resolution atmosphere can hold more moisture; as (‘grid size’) of a few hundred kilometres. water vapour is a greenhouse gas, this en- Th is is insuffi cient for resolving variable hances the initial warming. Possible changes landforms and other physiographical details in clouds are another key feedback. Th e sign that have a signifi cant eff ect on the near- of the overall climate sensitivity is robustly surface climate in many regions. Global known (positive, i.e. feedback enhances the model results are therefore applied to change due to some initiating factor, such as regions by various downscaling techniques emis sions), but its magnitude is generally (Rummukainen, 2010) such as statistical only known within a range of values. Th e models and regional climate models. Th e range of climate sensitivity in climate models latter is also known as dynamic downscaling. overlaps with the body of estimates based on Th e global climate modelling community historical and con temporary climate vari- has a long tradition of organizing co- ations, which pro vides confi dence in the ordinated simulation experiments that span models and their results. many climate models and diff erent sets of simulations. Many of the results in the Fourth Assessment Report of the IPCC 1.2.4 Climate models (Intergovernmental Panel on Climate Change; Meehl et al., 2007) came from the Climate models are sophisticated simulation so-called CMIP3 coordinated study, which models that build on the physical, chemical was followed by CMIP5 (Taylor et al., 2012). and biological understanding of the climate Coordinated regional climate model studies system, written in computer code. Th ere are are fewer but have, during the past few today quite a few global and regional climate years, emerged for several regions, not least models in the world, con stantly under Europe (Christensen and Christensen, 2007; further development, evalu ation and in use Kjellström et al., 2013), the Americas in research. Th e majority of climate models (Menendez et al., 2010; Mearns et al., 2012) have interacting components for the and Africa (Paeth et al., 2011). Coordinated atmosphere, the ocean and the land surface, studies of course provide more information but there are also models with interactive for the characterization of model-related carbon cycle and vegetation com ponents, as uncertainties, either by co-consideration of well as some with yet additional climate all results or by allowing a specifi c scenario system com ponents. Th e latter are today to be tested in a wider context, including known as ‘Earth System Models’. In the case how it compares with other scenarios. of models that do not carry a vegetation Advanced climate models are based on component, relevant properties are pre- fundamental physical laws. Th is enables scribed. their use in projections of the future beyond While climate models do exhibit various the observed period. Th ere are limitations biases, they also perform well in many on model resolution, as mentioned above, respects (Randall et al., 2007), including the meaning that small-scale processes that overall global and regional climate char- cannot be resolved have to be parameterized acteristics and the reproduction of observed (i.e. represented with approximate descrip- changes over time. tions). For example, cloud formation can- Global climate models are fundamental not be simulated explicitly in climate models when considering the response of the as it ultimately involves very detailed 10 M. Rummukainen

mechanisms. Rather, it may be para- roughly a doubling of the warming until the meterized in terms of relevant large-scale beginning of the 2000s. Th ere is not, ambient conditions in the models. Para- however, an absence of ongoing regional meterization is, however, also based on the changes before clear signals emerge; rather, physical understanding of the involved regional climates undergo transitions that processes. may manifest themselves earlier as changes Parameterizations are formulated in in, for example, the likelihood of extreme somewhat diff erent ways in diff erent climate events (Stott et al., 2004; Jaeger et al., 2008), models. Th is explains why climate models before the mean climate shows a signifi cant as a whole exhibit a range of climate response. sensitivities. Th is range overlaps observational estimates. 1.3 Projections

1.2.5 Internal variability 1.3.1 Temperature

Finally, the climate system is non-linear. Temperature change is a fundamental char- Th is manifests itself in ubiquitous internal acteristic of climate change (‘global warming’ variability within the climate system, is often used synonymously with the resulting in inter-annual variability and also present-day ‘climate change’). Th e observed variability at the decadal scale. Th e global global mean change since the pre-industrial mean temperature, for example, exhibits era is large compared to variability over some inter-annual variability in concert comparable timescales, and now amounts to with the large-scale interaction between the c.0.8–0.9°C. To keep the global mean ocean and the atmosphere in the Pacifi c, temperature rise under 2°C has been agreed known as El Niño–Southern Oscillation as the international target under the UN (ENSO). ENSO also has various strong Framework Convention on Climate Change regional signals around the world of (UNFCCC). However, the present evolution anomalous warmth and coolness, as well as of emissions is not aligned with emissions unusually wet and dry conditions. Diff erent pathways that might provide a likely chance variability patterns characterize yet other of meeting the two-degree goal (e.g. Peters world regions, including the Arctic and et al., 2013), suggesting that global warming North Atlantic Oscillations (AO, NAO; may well come to exceed this UNFCCC Th ompson and Wallace, 1998), the Pacifi c- target. Th e majority of climate change North American Pattern (PNA), as well as projections to date build on scenarios that the more regular monsoon circulations. do not include specifi c new climate policy Th e presence of signifi cant regional-scale measures and, consequently, result in a climate variability implies that, to begin larger warming than the two-degree goal. with, while climate change is indisputably Th e IPCC (2007) Fourth Assessment Report discernible at the large scale, it still may contained projected global warming results remain within regional-scale variability, that ranged from around 1°C to more than meaning that it may be more diffi cult to 6°C for the period between the late 20th identify conclusively at this scale. Th e same century and the late 21st century, with con- applies to climate projections and, consideration of diff erent emissions scenarios, sequently, the emergence of statistically climate models and information on climate signifi cant change occurs later in many change impacts on the carbon cycle. When regions than in the global mean (Giorgi and additionally considering the observed warm- Bi, 2009; Kjellström et al., 2013). Mahlstein ing since the pre-industrial until the late et al. (2012) fi nd, for example, that 20th century, the same projected change in statistically signifi cant regional precipitation temperature increases to c.1.5–7°C. changes emerge only once global mean Th e climate system response to forcing is warming climbs above 1.4°C, which is not uniform. While the overall pattern due Climate Projections for 2050 11

to emissions is one of warming, some globe, as evident from Plate 1 (see also, for regions will warm more (or less) than others, example, Solomon et al., 2009). Regional and thus more (or less) than the global mean changes are often larger or smaller than the change (see Plate 1). For example, a 2°C global mean change. Th ere is a distinct large- global mean warming would imply tempera- scale pattern that is coined ‘wet gets wetter’ ture increases larger than 2°C over land and ‘dry gets drier’ (cf. Held and Soden, regions. 2006). Although there are exceptions to Changes in the average temperature this, it by and large summarizes the big emerge over time in a relatively gradual picture well. Consequently, precipitation is manner. Changes in variability, and not least projected to increase at high and middle in extremes, can, however, manifest them- latitudes, decrease in the subtropical regions selves in more complicated ways. Intuitively, and increase in parts of the tropics. In the and what is also evident in climate pro- transition zones between these divergent jections, is that warm extremes become more patterns, the projected change is very small commonplace, whereas cold extremes less so or of insignifi cant magnitude. Th e exact (e.g. Zwiers et al., 2011; Orlowski and location of the transition regions varies to Seneviratne, 2012; Rum mukainen, 2012). It some extent between models and pro- is also characteristic that in areas in which jections. Th us, in the aff ected regions, while there is a reduction in seasonal snow cover, some projections may suggest an increase, such as the high northern latitudes, the others can show a decrease. reduction of cold extremes exceeds the A general increase in the occurrence of wintertime mean temperature change. Cor- heavy precipitation is, however, a typical respondingly, in the relatively dry subtropical result both for regions in which precipitation areas that experience increasing dryness, on average increases and for regions in changes in warm extremes exceed the which precipitation on average decreases. average regional temperature change (e.g. Th ere are many measures for extreme Kharin et al., 2013). precipitation. For example, such heavy As extremes manifest themselves in a precipitation events that at the end of the more or less sporadic fashion, changes in 20th century had a return period of 20 years them are more diffi cult to pinpoint than are projected to become 1-in-15- to 1-in-10- those of climate means (Trenberth, 2012). year events by around 2050 across most of Extremes can also change in terms of their the global land area (IPCC, 2012); that is, return period or likelihood of occurrence, with a rate of increase that is twice or more magnitude, geographical distribution, and the rate of the global mean precipitation so on. When posing the question of whether increase (Kharin et al., 2013). Th e un - extreme events will change in ways that certainty due to climate model quality is impact a specifi c sector or region, the larger for the tropics than for many other vulnerability of the activity or the location regions. Climate projections tend to exhibit needs to be specifi ed. Th e use of indices may large increases in extreme precipitation be helpful (Sillman and Roeckner, 2008; compared to changes in average precipitation Zhang et al., 2011). (Rummukainen, 2012; Kharin et al., 2013; Sillman et al., 2013). Precipitation is a basic measure of hydrological conditions, but does not wholly 1.3.2 Precipitation describe issues relating to water availability; information is also needed on evapo- Global precipitation increases with global transpiration, soil moisture, drought risks, warming. Results suggest that the increase runoff , etc. For example, there are studies in the global mean of precipitation is around that indicate an increasing risk of drought in 2% for each 1°C rise in temperature. Th e subtropical regions in the Americas, projected changes are non-uniform over the southern Europe, northern and southern 12 M. Rummukainen

Africa, South-east Asia and Australia is important for regions in which such (Dai, 2011; IPCC, 2012; Orlowsky and variability plays a signifi cant role in shaping Seneviratne, 2012). the regional climate (e.g. van Haren et al., 2013). Complementary regional-scale climate projections are carried out with downscaling, either by means of regional 1.3.3 Other aspects climate models (Rummukainen, 2010) or statistical downscaling (Maraun et al., 2010). Temperature and precipitation are two Downscaling attempts to capture better the fundamental aspects of the climate we infl uence of variable orography and land– experience. Th ere are also a variety of other sea distribution on the regional climate than variables and processes that intimately what is feasible to achieve with global aff ect us, such as cloudiness, soil moisture, models. Consequently, for many climate evapotranspiration, snow, glaciers and sea change impact studies, downscaled climate ice, wind and sea level. Characterization of projections can be a better starting point the climate also involves the consideration than the direct results of global climate of sequences of events and phenomena projections. such as, for example, drought, fl ooding, For example, Kjellström et al. (2013) storms and heatwaves. Likewise, character- analysed results from 21 recent regional ization of the climate concerns, in addition climate models for Europe. Even though to average conditions, also variability these had been forced by diff erent global patterns and extremes (IPCC, 2007, 2012; models, the projections gave very similar Rummukainen, 2012). While climate patterns of change for both temperature and projections can provide information on all precipitation (see Plate 2). Th e largest of these aspects, a comprehensive account wintertime changes occur in the north-east is beyond this chapter. Also, which aspects and the largest summertime ones in the are pertin ent to consider depends on the south. Precipitation tends to increase in the question in hand: for example, the kind of north and decrease in the south. However, climate impact or region of interest. there are also models that show small to Seasonality related to agriculture, for insignifi cant changes in large parts of example, follows temperature in Europe, Europe, and models that suggest a general while it follows the succession of wet and wetting. Th ese fi ndings largely confi rm dry periods in Africa. earlier regional projection results for Europe (e.g. Christensen and Christensen, 2007; Déqué et al., 2012). 1.4 Regional Patterns of Change A similar analysis for Africa is shown in Plate 3. In North Africa, warming is greater Global climate model projections also pro- in the summer than in the winter. Th ere is a vide information on regional-scale climate. similar feature in the south of Africa. Plate 1 gives a fi rst impression of regional Warming for most of the models here ranges patterns of projected temperature and from around 1°C or slightly less to somewhat precipitation change, relative to the overall above 2°C. Th e range of precipitation global mean warming amount. changes projected by regional climate However, the detail in global climate models (RCMs) is similar to the European model projections is constrained by model case (Plate 2), in the sense that it spans from resolution, which in most cases corresponds a general drying to a general wetting. Th e to a few hundreds of kilometres (Masson RCM median result suggests drying in both and Knutti, 2011; Räisänen and Ylhäisi, the north and the south of Africa, and either 2011). Information on the quality of the an increase or no change in between these models in simulating large-scale variability areas. Climate Projections for 2050 13

1.5 Circulation Patterns and Regional continued reduction of the Arctic sea ice Changes cover may counteract the eff ect of the overall warming on the occurrence of cold winter Internal variability is a ubiquitous aspect of months in Europe and concurrent mild the climate system. Its specifi c regional winters across North America. Th is does not manifestations can often be analysed in mean an expectation of more cold winters in terms of circulation patterns or ‘large-scale Europe, however, but rather that cold variability modes’. For example, diff erent winters will still occur even when overall phases of ENSO lead to signifi cant regional warming proceeds. temperature and precipitation anomalies in Overall, regional-scale climate in many many parts of the world. Inter-annual parts of the world is shaped not only by variability in the North Atlantic, Europe and global-scale constraints but also by the the Arctic region occurs in concert with the action of circulation patterns; the latter North Atlantic Oscillation and the Arctic often warrant special attention in the Oscillation, and manifests itself as, not analysis of regional climate change pro- least, inter-annual variability in general jections (Deser et al., 2012). cold-season weather. In monsoon regions, such as South-east Asia and Western Africa, the seasonally changing temperature con- 1.6 Discussion and Conclusion trast between the land and the sea generates a distinct variability of regional precipitation. Climate change is of global and regional Under climate change, however, some of the concern. In addition to general warming, characteristics of circulation patterns may changes are expected in precipitation change. Th is would imply regional climate patterns and other aspects, both on average change that further deviates from the global and in terms of variability and extreme mean, in addition to the general larger events. Changes that well exceed climate warming over land than over sea, etc. (cf. variability far back in time, and certainly Plate 1). over the history of modern society, are to be While individual models may project expected. Th is underlines the need for various changes in circulation patterns as a knowledge on how the future can unfold, in result of climate change, global climate order to anticipate the impacts and to be projections to date do not collectively able to prepare for them. Climate projections suggest major shifts in ENSO, NAO and off er a means to do this. some of the other comparable modes (IPCC, A pertinent question for analyses and 2007). Precipitation associated with mon- impact assessments is ‘which climate model soons is projected to increase in general, as and projection to choose’. Unfortunately, well as the overall global area that is aff ected there is no specifi c answer. Rather, one by monsoons (Hsu et al., 2012), due to higher needs to recognize the sources of uncertainty sea surface temperature and atmospheric and, as much as possible, look at many water vapour content resulting from global projections from many climate models, warming. based on diff erent emissions scenarios. In More recently, it has been postulated that the case of it being prohibitive to account for the retreat of sea ice in the Arctic region may large sets of scenarios, the evaluation of aff ect atmospheric circulation and promote climate models may provide guidance for the occurrence of more persistent weather choosing a smaller set of models and pro- patterns, such as extreme winters and jections. For example, one could perhaps summers at the high and mid-latitudes of exclude models which exhibit larger biases the northern hemisphere (Francis and in variables that are especially crucial for the Vavrus, 2012; Liu et al., 2012). Climate impact study in hand. For the early part of models suggest that such a link may exist the 21st century, projections are relatively and play some role during the 21st century similar across many emissions scenarios; (Yang and Christensen, 2012). Th e expected and one could consider focusing on one or at 14 M. Rummukainen

most a few emissions scenarios. In any case, In the end, of course, the intended use of consideration of the results from more than climate projections, such as in agricultural one model and/or projection is always impact assessment, needs to guide the recommended. While use of a subset of considerations. High-resolution information models and projections does not necessarily may be preferred, in which case downscaled suffi ce for quantifi cation of scenario information, be it from statistical or uncertainty, it can still provide a useful dynamical approaches, is probably needed. reminder that scenarios and projections are Th e assessment and impact model at hand possible unfolding futures that are subject may pose constraints on whether individual to uncertainty, rather than defi nitive fore- projections or ensemble-based results can casts. be used. Nevertheless, proper consideration Climate projection results are often of climate projections necessarily requires similar when it comes to the direction of the insights into their basis and underlying projected changes, be these of increase, scenario assumptions. decrease or no evident change. Th e size of projected change, however, varies more. Th is is due in part to diff erences in climate Note sensitivity, i.e. in the response to a given forcing represented in models (in other 1 The defi nition of climate sensitivity refers to the words, in the underlying process descrip- long-term (equilibrium) global mean temperature tions). Some of the variation across models rise for a doubling of the atmospheric carbon can be attributed to the simulated internal dioxide content. A specifi c climate scenario may variability. Nevertheless, the magnitude of feature an increase in the atmospheric carbon change characteristically increases with dioxide concentration that is either smaller or larger than a doubling. The value of the climate fossil fuel emissions and land-use change, sensitivity should thus not be confused with a and thus also over time as long as these specifi c climate change/global warming remain unabated. scenario. Another concept is the ‘transient One way to condense information from climate response’, which refers to the warming multiple models and projections is to that manifests itself around the time when the consider multi-models (ensembles). Analysis atmospheric carbon dioxide concentration doubles. The climate sensitivity is larger than the of multi-model means helps to highlight transient climate response, which is due to the results that are consistent across the models, slow progression of warming signals to spread although this occurs at the expense of sup- in the ocean. pressing outliers. For example, the latitude zones that border the higher latitude regions with a projected consistent precipitation References increase, and the subtropical regions with a projected consistent pre cipitation decrease, Alessandri, A., Borrelli, A., Navarra, A., Arribas, A., have a ‘no change’ appearance, while specifi c Déqué, M., Rogel, P., et al. (2011) Evaluation of projections may exhibit either increases or probabilistic quality and value of the decreases. Outliers may need to be considered ENSEMBLES multimodel seasonal forecasts: for impact assessments, as they may comparison with DEMETER. Monthly Weather represent extreme responses and thus give at Review 139, 581–607. least a partial idea of ‘best case’ and ‘worst Christensen, J.H.C. and Christensen, O.B.C. (2007) case’ scenarios. Th us, multi-model mean A summary of the PRUDENCE model results need to be amended with con- projections of changes in European climate by sideration of either some individual pro- the end of this century. Climatic Change 81, 7–30. jections, or the model spread. Th e pursuit of Dai, A. (2011) Drought under global warming: a probabilistic projection analysis of global and review. Wiley Interdisciplinary Reviews: Climate regional projections is a more refi ned method Change 2, 45–65. addressing the same problem (e.g. Déqué and Déqué, M. and Somot, S. (2010) Weighted Somot, 2010; Alessandri et al., 2011). frequency distributions express modelling un - Climate Projections for 2050 15

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