THE CONTRIBUTION OF BIODIVERSITY FOR FOOD AND AGRICULTURE TO THE RESILIENCE OF PRODUCTION SYSTEMSThematic Study for The State of the World’s Biodiversity for Food and Agriculture

THEMATIC STUDY

Ashley DuVal1, Dunja Mijatovic2 and Toby Hodgkin2

1 Scientific Consultant2 Platform for Agrobiodiversity Research

THE CONTRIBUTION OF BIODIVERSITY FOR FOOD AND AGRICULTURE TO THE RESILIENCE OF PRODUCTION SYSTEMSThematic Study for The State of the World’s Biodiversity for Food and Agriculture

COMMISSION ON GENETIC RESOURCES FOR FOOD AND AGRICULTURE FOOD AND AGRICULTURE ORGANIZATION OF THE UNITED NATIONS

Rome, 2019

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Required citation:DuVal, A., Mijatovic, D. & Hodgkin, T. 2019. The contribution of biodiversity for food and agriculture to the resilience of production systems –Thematic Study for The State of the World’s Biodiversity for Food and Agriculture. FAO, Rome. 85 pp. Licence: CC BY-NC-SA 3.0 IGO.

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Contents

Acknowledgements ......................................................................................................................... vExecutive summary .....................................................................................................................vii

1. Introduction ........................................................................................................................... 1

2. The roles of biodiversity in sustainable food production .................................................. 3

3. Resilience in production systems ........................................................................................... 5

4. Methodology .............................................................................................................................. 9

5. Results .....................................................................................................................................11 5.1. Genetic diversity ...........................................................................................................11

5.1.1. Crops .........................................................................................................................11 5.1.2. Forest and tree crops .............................................................................................. 15 5.1.3. Livestock .................................................................................................................. 17 5.1.4. Aquatic organisms ...................................................................................................18

5.2. Species diversity, including farming system diversity ............................................ 21 5.2.1. Crop species mixtures ............................................................................................ 21 5.2.2. Agroforestry and mixed species forests and plantations .................................... 23 5.2.3. Species diversity in livestock ................................................................................. 23 5.2.4. Integrated crop–livestock systems ........................................................................ 24 5.2.5. Integrated and multi-trophic aquaculture ........................................................... 24

5.3. Diversity at the landscape/seascape scale ................................................................. 26 5.3.1. Spatial diversification of crops across a landscape ............................................... 26 5.3.2. Forests, woodlots and silvopastoral systems ....................................................... 29 5.3.3. Rangeland management ......................................................................................... 30 5.3.4. Marine fisheries and wetlands ................................................................................31

5.4. Associated biodiversity ...............................................................................................31 5.4.1. Soil-associated biodiversity .................................................................................... 32 5.4.2. Pollinator biodiversity............................................................................................ 34 5.4.3. Associated biodiversity for fisheries ..................................................................... 35

6. Livelihoods, food security and nutrition ............................................................................ 39 6.1. Rural livelihoods ........................................................................................................... 39 6.2. Food security and nutrition ........................................................................................ 40

7. Conclusions ............................................................................................................................... 43 7.1. Main findings ................................................................................................................ 43

7.1.1. Resistance or tolerance to shocks and stresses ..................................................... 43 7.1.2. Adaptation and continued evolution ..................................................................... 43

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7.1.3. Stability of production systems and ecosystem services under multiple stresses ......................................................................................................................... 44

7.1.4. Recovery following disturbance ............................................................................ 44 7.2. Research and knowledge gaps .................................................................................... 44

7.2.1. Responses to and recovery from disturbances ..................................................... 44 7.2.2. Integrating across scales and components over time ........................................... 45 7.2.3. Achieving transformation towards diversity-rich production systems ............. 45

7.3. Recommendations ....................................................................................................... 45

Glossary ...................................................................................................................................... 49

References ......................................................................................................................................51

Tables

Table 1 Regulating and supporting ecosystem services provided by biodiversity for food and agriculture ......................................................................................... 1

Table 2 Social and ecological characteristics of resilience ................................................. 6

Table 3 Selected search terms used in screening literature on BFA and resilience ......... 9

Table 4. Contribution of genetic diversity to resilience in crops ...................................... 12

Table 5. Contributions of genetic diversity to resilience in trees ......................................14

Table 6. Contributions of genetic diversity to resilience in livestock breeds ...................16

Table 7. Contributions of genetic diversity to resilience in aquatic organisms ................19

Table 8. Contributions of species diversity to resilience in crops .................................... 20

Table 9. Contributions of species diversity to resilience in agroforestry systems and mixed species plantations .................................................................................... 22

Table 10. Contributions of species diversity to resilience in livestock ............................ 24

Table 11. Contributions of species diversity to resilience in integrated crop–livestock systems .................................................................................................................. 25

Table 12. Contributions of species diversity to resilience in integrated aquaculture systems .................................................................................................................. 26

Table 13. Contributions of diversification with crops at the landscape scale .................. 27

Table 14. Contributions of landscape scale interventions to resilience in forests, woodlots and silvopastoral systems ................................................................... 28

Table 15. Contributions of BFA to resilience in rangelands ............................................. 30

Table 16. Contributions of marine diversity to resilience ................................................. 32

Table 17. Contributions of soil diversity to resilience ....................................................... 34

Table 18. Contributions of pollinator diversity to resilience ............................................ 35

Table 19. Contributions of associated biodiversity in marine ecosystems to resilience 36

Table 20. Interactions between species, traits and resilience in a coral reef fishery ....... 36

Table 21. Main benefits of resilience-enhancing practices to livelihoods and food security .................................................................................................................. 39

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Acknowledgements

We would like to express our gratitude to Julie Bélanger for the support she provided throughout the process of conceptualizing, developing and revising this review. We are grateful to the many reviewers whose comments and revisions greatly improved upon the scope and content of this study, in particular Davide Albeggiani, Devin Bartley, Agnès Bernis-Fonteneau, Linda Collette, Ladina Knapp, Damiano Luchetti, Alexandre Meybeck, Dafydd Pilling, Manuel Pomar, Marcela Portocarrero-Aya, Suzanne Redfern, Beate Scherf, Doris Soto, Kim-Anh Tempelman, Miriam Widmer (Food and Agriculture Organization), Roger Pullin, Selena Ahmed (Montana State University), Louise E. Jackson (University of California, Davis), Brenda Lin (Commonwealth Scientific and Industrial Research Organisation), Ann Thrupp (University of California, Berkeley) and Pablo Tittonell (Instituto Nacional de Tecnologia Agropecuaria, Argentina).

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Executive summary This thematic study, prepared as a contribution to The State of the World’s Biodiversity for Food and Agriculture, reviews the available information on the contribution of biodiversity for food and agriculture1 (BFA) to the resilience of crop, livestock, forest, fishery and aquaculture production systems to environmental change and uncertainty. It:

• summarizes evidence that links BFA at genetic, species and landscape levels to the resilience of production systems;

• discusses the contributions of BFA-based resilience-strengthening strategies to livelihoods, food security and nutrition; and

• identifies strategies for using BFA to enhance resilience.Environmental changes and uncertainty are increasingly significant features of

production systems. The International Panel on Climate Change (IPCC) has reported that all aspects of food security are potentially affected by climate change, including food production, access, consumption and price stability. Rural areas are expected to experience major impacts on water availability and supply, food security, infrastructure and agricultural incomes. Significant impacts are also expected on global marine species, coastal production areas, available surface water, and crop and animal productivity and production. Increasing the resilience of production systems is therefore vital.

Production environments can be viewed as complex social–ecological systems (SES), in which social and ecological dimensions are connected through management, consumption and extractive practices that influence the characteristics of BFA. In this study, resilience is defined as the capacity of these systems to absorb stresses and shocks, maintain function in the face of stresses and variability related to environmental change, and evolve into systems capable of withstanding a wide range of future conditions.

The study reviews peer-reviewed and grey literature, selected through key word searches, that provides evidence as to the relationship between BFA and resilience. The criteria for inclusion of case studies ensured a focus on those that: (i) describe a problem of increasing stress or sudden change; (ii) include a description of genetic, species or ecosystem diversity; and (iii) consider relationships between diversity and the absorption of stress or shock, maintenance of function under increasing stress, recovery following disturbances or adaptation to change in production systems.

The review shows that BFA contributes to resilience of production systems by maintaining stability in the context of increasing occurrence of shocks and stresses, enabling adaptation, and supporting recovery from disturbances. These contributions are interrelated and involve interactions between genetic, species and ecosystem diversity at different spatial scales.

The review identifies a number of important knowledge gaps, including: (i) a lack of information on the contribution of BFA to recovery from disturbances and how BFA can be better harnessed in the restoration of ecosystem services, particularly in intensive and/or industrialized production systems; (ii) a lack of studies that address more than one component of BFA and are undertaken over longer periods; and (iii) a lack of assessments of effective strategies for promoting wide-scale adoption of resilience-strengthening practices.

The review identifies a number of ways in which BFA contributes to enhanced resilience. These can be grouped into three broad categories that characterize the role of

1 Biodiversity for food and agriculture (BFA) includes the variety and variability of animals, plants and micro-organ-isms at the genetic, species and ecosystem levels that sustain the ecosystem structures, functions and processes in and around production systems, and that provide food and non-food agricultural products.

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BFA in resilience at different scales. These three approaches are interrelated and mutually supportive of the resilience of production systems:

1. conservation and use of genetic and species diversity to support adaptation and continued evolution, including the characterization and evaluation of traits linked with resilience;

2 diversification of production-system components to manage risks and mitigate the impact of climate change and variability on production; and

3. habitat restoration for landscape/seascape complexity to support the supply of ecosystem services and the capacity of production systems to absorb and recover from disturbance or adapt to future conditions.

Based on the findings of this study, the following recommendations for harnessing BFA to increase the resilience of production systems are offered:

1. support adaptation and continued evolution through in situ conservation of a diversity of tree, aquatic and crop wild relatives as well as traditional breeds and varieties of livestock and crops;

2. diversify farms and in fields, both by conserving local biological resources and by improving access to new resources and associated knowledge, targeting components of BFA (crops, trees, livestock and aquatic species) known to increase the range of possible responses to variable and changing climatic conditions;

3. adopt practices that support beneficial ecological interactions (complementarity), the diversity needed to respond to change (response diversity) and the diversity within functional groups (groups of organisms that carry out similar functions within an ecosystem, e.g. groups of soil biota, pollinators);

4. maintain the complexity and heterogeneity of landscapes/seascapes that underpin the sustained flow of ecosystem services, support regeneration after disturbances and provide habitats for associated biodiversity, including wild plants animals and micro-organisms;

5. enable mobility and migration (natural and assisted) and the movement of organisms, especially preadapted populations, ecotypes, breeds, etc., to facilitate adaptation to projected conditions and new environments;

6. adopt participatory and transdisciplinary approaches to research and conservation within an integrative social-ecological systems framework aiming to support the development and promotion of locally appropriate resilience-strengthening strategies that build on or take account of local knowledge;

7. strengthen research, including: (i) studies of the contribution of BFA to the resilience of production systems and especially to recovery from multiple stresses and shocks; (ii) studies of resilience-promoting strategies that integrate diverse components of BFA at different scales; and (iii) long-term studies that assess the contribution of BFA to resilience over a sufficient period of time to capture medium- and long-term outcomes; and

8. increase institutional and policy support for the wider adoption of diversity-rich practices that contribute to resilience.

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1. Introduction

This thematic study reviews the available information on the contribution of biodiversity for food and agriculture (BFA) to the resilience of crop, livestock, forest, fishery and aquaculture production systems to environmental change, variability and uncertainty.1 BFA includes the variety and variability of animals, plants and micro-organisms at the genetic, species and ecosystem levels that sustain the ecosystem structures, functions and processes in and around production systems, and that provide food and non-food agricultural products. Thus, BFA includes species, varieties, breeds and populations of crops and livestock, fish and other harvested wild species, and the wild relatives of domesticated species. It also includes what is referred to in The State of the World’s Biodiversity for Food and Agriculture as “associated biodiversity”, i.e. species that contribute regulating and supporting ecosystem services to production systems, for example by pollinating plants, controlling pests and diseases, forming and maintaining healthy soils, regulating water supplies and maintaining water quality (Table 1). Throughout the study, the various biotic elements characteristic of different production systems are referred to as “components of BFA”.

Environmental changes and increasing variability are having significant impacts on agriculture, including crop and animal production, forestry, fisheries and aquaculture (IPCC, 2014). Multiple interacting and sometimes mutually reinforcing stressors are eroding BFA and

the ecosystem services upon which local livelihoods and food security depend. Anthropogenic stressors such as the destruction, fragmentation and degradation of natural habitats caused by deforestation, overgrazing or overfishing, often exacerbate impacts. Conversely, the use or conservation of BFA can promote mitigation and adaptation to climate change (Lin, 2011; Isbell et al., 2015; Gaudin et al., 2015), increase the sustainability of production environments (FAO/PAR, 2011; Bommarco, Vico and Hallin 2018) and improve food security, for instance by increasing the diversity of diets (Frison, Cherfas and Hodgkin, 2011; Thomson and Fanzo, 2015; Garibaldi et al., 2016).

Resilience is an important feature of production systems (IAASTD, 2009), particularly in the context of environmental change (IPCC, 2014). The concept of resilience derives from ecological research (Holling, 1973) but has expanded to encompass social and economic perspectives (Walker et al., 2002, 2006; Folke et al., 2004, 2010). Resilience can thus be considered a property of social ecological systems (SES). SES are complex adaptive systems, and the social-ecological resilience approach provides a way to understand and address their dynamics (Folke et al., 2016). Production systems can be seen as SES in which social

1 We consider environmental change and uncertainty to include climatic change and variability, shocks and stressors, slow onset events, and environmental degradation.

Table 1. Regulating and supporting ecosystem services provided by biodiversity for food and agriculture1

Regulating Supporting

Climate regulation

Natural-hazard regulation

Pest and disease regulation

Pollination

Nutrient cycling

Soil formation and protection

Water cycling

Habitat provisioning

1 Based upon Guidelines for the preparation of the Country Reports for The State of the World’s Biodiversity for Food and Agriculture. The classification of ecosystem services in this report is consistent with the Millennium Ecosystem Assessment (2005).

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and ecological dimensions are connected through management, consumption and extractive practices that influence the characteristics of BFA (see Section 3).

For the purposes of this study, resilience is defined as the capacity of a system to absorb stresses and shocks, maintain function in the face of stresses and variability related to environmental change, and evolve into a system capable of withstanding a wide range of future conditions. The study considers the growing body of literature on the contributions of BFA to the resilience of production systems in the context of environmental changes, including stresses, shocks and variability, through the social-ecological resilience lens. More specifically, it aims to:

• summarize evidence regarding the contribution of BFA to the resilience of production systems and their various components – crops, livestock, aquatic organisms, trees and associated biodiversity – at the scales of genetic and species diversity (Section 5);

• review the ways in which the contribution of BFA to resilience can strengthen livelihoods and improve food security and nutrition (Section 6); and

• identify strategies for using BFA to enhance the resilience of production systems at different levels (e.g. genetic or species) and scales (e.g. field/pond, farm or landscape/seascape) (Section 7).

The findings of the literature review are presented in Section 5. Section 6 considers the interrelationships between BFA’s contributions to resilience and livelihoods, food security and nutrition. Section 7 summarizes the main findings of the review, identifies some major gaps in current knowledge and suggests actions that can help improve the use of BFA to support resilience.

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2. Production systems in the context of environmental change and uncertainty

Production systems are vulnerable to a range of global drivers of change, of which climate change is particularly important. While the specific local effects of broad climatic changes at the global level will depend on unique local conditions, the fifth IPCC assessment report (IPCC, 2014) draws some compelling general conclusions regarding impacts on agriculture and food production. For example, it notes that:

• all aspects of food security are potentially affected by climate change, including food availability, access to food, nutrient utilization and stability of food supply;

• rural areas are expected to experience major impacts on water availability and supply, food security, infrastructure and agricultural incomes, including shifts in the production areas of food and non-food crops around the world;

• redistribution of marine species and reduction of marine biodiversity in sensitive regions will challenge the sustainability of fisheries productivity and other ecosystem services, especially at low latitudes;

• marine ecosystems, especially coral reefs and polar ecosystems, are at risk from ocean acidification;

• coastal systems and low-lying areas will increasingly experience submergence, flooding and erosion throughout the twenty-first century and beyond due to rising sea levels;

• climate change is projected to reduce renewable surface water and groundwater resources in most dry subtropical regions; and

• negative impacts on average crop yields and increases in yield variability are already occurring.

These conclusions take into account the evidence that production systems are being affected by increased climatic variability, including erratic and unpredictable rainfall, shifting seasonal patterns, more frequent extreme weather events and rising temperatures (Salinger, Sivakumar and Motha, 2005; Balaghi et al., 2010; Vermeulen, Campbell and Ingram, 2012). These changes exacerbate pest damage (Birch et al., 2011) and alter the distributions of pests and pathogens (Bebber, Ramotowski and Gurr, 2013). Rising temperatures affect soil properties both directly and indirectly, for example via the evaporation of soil moisture (Kotschi, 2006). While increased CO2 concentrations may enhance photosynthetic rates in some plants in some regions, the plants will not benefit unless soil composition and water availability allow increased nutrient requirements to be met (Dwivedi et al., 2013).

Some of the better-described threats to components of BFA are described below. For a more detailed discussion, see FAO (2015).

• Crops: yields are likely to decrease at low latitudes, with significant effects on rice, maize and wheat – the three primary staple crops of the world (Lobell et al., 2008; Rosenzweig et al., 2014; Challinor et al., 2014). The geographical ranges of many pests and diseases will shift, as will those of many useful crop-associated species, including pollinators and seed dispersers (FAO, 2015). Many crop wild relatives will be at risk as current conditions change, with an estimated 16–22 percent threatened by extinction in the next 50 years (Jarvis, Lane and Hijmans, 2008).

• Forest trees: climate change, combined with deforestation, contributes to the progressive depletion of tree biodiversity. Changes in climate will result in relatively rapid changes in the suitable growing ranges of particular tree species (Petit, Hu and Dicks, 2008; Dawson et al., 2010). In the tropics, altered precipitation patterns can create barriers to genetic exchange within tree species (Muchugi et al., 2006, 2008).

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• Livestock: stressors linked to climate change that will affect livestock production include more frequent and more severe extreme weather events, changes in the ranges of diseases and parasites, and reductions in the availability of feed and water (Thornton et al., 2009; FAO, 2013). Reduced precipitation and increased frequency of droughts will impair milk and meat production and result in the loss of livestock (Webb and Reardon, 1992; Mutekwa, 2009).

• Aquatic species: coastal and offshore fisheries are highly vulnerable to climate change and overfishing and the consequent extinction of unique subpopulations and overall loss of genetic diversity (Grant, 2007; Weatherdon et al., 2016; Pullin and White, 2011). Changes in aquatic habitats (e.g. in temperature and levels of dissolved oxygen) can alter the feeding, breeding, growth and geographic distribution of fish (Brander, 2010). Coral reefs, which provide habitat and breeding grounds for many species targeted by capture fisheries, are vulnerable to changes in temperature and acidity and to sea-level rise, which are being exacerbated by overfishing, pollution and disturbances to community composition and trophic structure (Cinner et al., 2013; D’agata et al., 2014). Rising temperatures have been linked with higher metabolic rates and quicker development in aquatic organisms and, in the case of aquatic animals, with smaller body sizes (Sheridan and Bickford, 2011). Rising sea levels will displace brackish and freshwater river deltas, with repercussions for freshwater aquaculture and for wetland habitats (De Young et al., 2012).

One major impact that climate change, in combination with other drivers of change, is having on production systems is an increase in vulnerability to biotic and abiotic stresses and uncertainty. Vulnerability can be regarded as the likelihood that an event or set of events will have a negative impact on a particular feature of the production system (e.g. the likelihood that drought will reduce yield or that a particular pest or disease will cause major losses in production).

The available evidence suggests that the vulnerability of many production systems to climate change and environmental uncertainty is increasing as a result of other factors, including the simplification of landscapes, the loss of associated biodiversity and the loss of species and genetic diversity in crop, livestock, fish and forest-tree populations. Examples of the damage that can be caused by reduced genetic diversity include the major losses of taro production that occurred in Samoa in the 1990s (Hunter et al., 1998) and the losses of maize production that occurred in the United States of America in the 1970s as a result of the uniformity of maize varieties in the face of attacks by Helminthosporium maydis (Gracen, Grogan and Forster, 1972).

The vulnerability of livestock production systems to diseases (including zoonotic diseases that have severe consequences for human health) is being increased by (inter alia) climate change and greater genetic uniformity in livestock populations (Otte et al., 2007; FAO, 2013). Land-use change, changes in agricultural and food-production practices and wildlife hunting, collectively, accounted for almost half of all the zoonotic diseases that emerged in humans between 1940 and 2004 (Keesing et al., 2010). Examples of increased vulnerability as a result of the loss of associated biodiversity include the reduced agricultural yields caused by pollinator deficits and reduced soil quality as a result of the loss of organic matter and soil organisms (Garibaldi et al., 2013; Brussaard, de Ruiter and Brown, 2007; Cardinale et al., 2012; FAO/PAR, 2011).

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3. Resilience in production systems

The concept of resilience emerged in the ecological literature during the 1960s and 1970s to challenge the equilibrium view of the ecosystem and emphasize non-linear dynamics, thresholds, uncertainty, continuous change and interactions across temporal and spatial scales. The relationship between biodiversity and resilience has been studied by ecologists for over four decades, often with the aim of informing policies and practices for ecosystem management. In the last decade or so, resilience science has broadened into an interdisciplinary discourse that focuses on the interactions of humans and ecosystems via linked SES (Folke, 2006). The concept of social-ecological resilience has been applied to a range of production systems (Darnhofer, Fairweather and Moller, 2010; Darnhofer et al., 2010; Berkes, 2012; Kremen and Miles, 2012; Cabell and Oelofse, 2012; Haider, Quinlan and Peterson, 2012). SES are characterized by complex interactions across multiple spatial, temporal and organizational scales. Resilience of SES has been described as their capacity to continually change, adapt and transform in response to external drivers and internal processes through innovation (Folke et al., 2010). Resilience is multifaceted. Interactions between the properties of SES that contribute to resilient outcomes are described in the following paragraphs.

The functioning of SES is governed by a combination of (1) management interventions reflecting various social, cultural, economic and institutional factors and constraints and (2) the abiotic and biotic features of the environment. Ultimately, resilience of SES is conferred by interactions between their social and ecological dimensions (Table 2). The social dimension includes learning and innovation, social networks, institutions, governance and adaptive management. Learning and innovation (Berkes, Colding and Folke, 2000) and the ability to combine different types of knowledge (e.g. traditional and scientific) through management practices and decision-making at all levels (Folke et al., 2010) are important aspects of resilience in SES.

Resilience in SES is not just about resistance to change, but also about recovery and adaptation (i.e. adjustments in response to new stresses) or even transformation at the household, community or country level (i.e. substantial changes to create a more sustainable system) (Berkes, Colding and Folke, eds, 2003; Walker et al., 2004; IFPRI, 2014). BFA has been identified as a potential contributor to absorptive or coping capacity (i.e. capacity to moderate or buffer the impacts of shocks) and to adaptive capacity (i.e. the preconditions necessary for a system to be able to adapt to disturbances) (Nelson, Adger and Brown, 2007).

Important ways in which BFA contributes to resilience include stabilizing production (Isbell et al., 2017), sustaining ecosystem functions (services) (Landis, 2017; Oliver et al., 2015) and enabling adaptation (Sgrò, Lowe and Hoffmann, 2011; Vigouroux et al., 2011; Bellon et al., 2017). While production may not always be directly correlated with biodiversity, biodiversity is an important factor in sustaining production over time (Hautier et al., 2014). Sustained production is related to capacity for ecological self-regulation (Table 2) – the ability of systems to recover and adjust and hence to sustain comparatively constant levels of productivity. Furthermore, resilience in production systems depends largely on the healthy functioning of ecosystems and the stable delivery of ecosystem services, many of which are provided by BFA (Table 1). The functioning of production systems depends on a complex array of organisms interlinked through food webs, nutrient cycling, pollination, seed dispersal and other ecological relationships. These ecological and biological interactions may at times be mediated by human interventions to achieve the specific objectives of the particular production system.

Other aspects of diversity of relevance to social-ecological resilience are functional diversity and response diversity (Table 2). Functional diversity (defined by Tilman et al.

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[2001] as the value and range of the functional traits of the organisms in a given ecosystem) affects aspects of ecosystem functioning including the provision of ecosystem services (Diaz et al., 2007). Functional diversity in managed or restored ecosystems contributes to their stability and resilience through time as multiple functional traits can help buffer ecosystems

Table 2. Social and ecological characteristics of resilience

Characteristic Contribution to social-ecological resilience

References

Ecological self-regulation

Stabilizing feedback mechanisms support recovery after stress and adaptation to internal and external change.

Sundkvist, Milestad and Jansson, 2005; Ewell, 1999; Jackson, 2002; Swift, Izac and van Noordwijk, 2004; Jacke and Toensmeier, 2005; Glover et al., 2010; McKey et al., 2010

Functional diversity and functional redundancy

Functional diversity and the functional redundancy of species within a functional group (a collection of species that perform the same ecological role or fill a similar niche), buffer stresses and enable recovery from them.

Altieri, 1999; Ewell, 1999; Berkes, Colding and Folke, 2003; Luck et al., 2003; Swift, Izac and van Noordwijk, 2004; Folke, 2006; Jackson, Pascual and Hodgkin, 2007; Di Falco and Chavas, 2008; Moonen and Barbieri, 2008; Chapin, Kofinas and Folke, 2009; Darnhofer, Fairweather and Moller, 2010; Darnhofer et al., 2010; IAASTD, 2009

Response diversity The range of responses within a functional group or among “redundant” elements contributes to an “insurance effect” and to adaptation.

Elmqvist et al., 2003; Mori, Furukawa and Sasaki, 2013; Cabell and Oelofse, 2012; Kahiluoto et al., 2014; Hakala et al., 2012

Spatial and temporal heterogeneity

Mosaic patterns of managed and unmanaged landscape/seascape, crop rotations and diverse cultivation practices support renewal and buffer stresses, and provide habitat for associated biodiversity.

Alcorn and Toledo, 1998; Devictor and Jiguet, 2007; Di Falco and Chavas, 2008;

Socially self-organized Communities self-organize through dynamic processes of personal and collective action to manage the land, biodiversity and water resources upon which they depend.

Levin, 1999; Holling, 2001; Milestad and Darnhofer, 2003; Atwell, Schulte and Westphal, 2010; McKey et al., 2010

Building natural capital Responsible use of local resources encourages the system to live within its means; this creates an agroecosystem that recycles waste, relies on healthy soil and conserves water.

Ewell, 1999; Milestad and Darnhofer, 2003; Robertson and Swinton, 2005; Naylor, 2009; Darnhofer, Fairweather and Moller, 2010; Darnhofer et al., 2010; Van Apeldoorn et al., 2011

Reflective and shared learning

Individuals and institutions learn from past experiences and present experimentation to anticipate change and create desirable futures.

Berkes, Colding and Folke, 2003; Darnhofer, Fairweather and Moller, 2010; Milestad et al., 2010; Shava et al., 2010

Autonomous and locally interdependent

The system has relative autonomy from exogenous (global) control and exhibits a high level of cooperation between individuals and institutions at the more local level.

Milestad and Darnhofer, 2003; Folke et al. 2005; Van Apeldoorn et al., 2011

Traditional knowledge The current configuration and future trajectories of systems are influenced and informed by past conditions and experiences.

Gunderson and Holling, eds, 2002; Cumming et al., 2005; Shava et al., 2010; van Apeldoorn et al., 2011

Source: Adapted from indicators described by Cabell and Oelofse (2012).

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against abiotic variation (Diaz et al., 2007; Cadotte, Carscadden and Mirotchnick, 2011). The loss of functional diversity in plants has been demonstrated to increase the vulnerability of ecosystems to stress and environmental change (Laliberté et al., 2010). The functional redundancy of organisms can provide an “insurance effect” – the loss of species performing a particular function is compensated for by other species that have a similar function. Functional redundancy corresponds to increased variation in responses within a functional group (Elmqvist et al., 2003), thereby contributing to response diversity (see below).

Response diversity refers to species assemblages, species and varieties that perform similar ecosystem functions but have different capacities to respond to disturbance or fluctuations. The variation in responses among species performing similar functions may be a key determinant of ecosystem and agroecosystem resilience to environmental change (Cabell and Oelofse, 2012; Mori, Furukawa and Sasaki, 2013; Kahiluoto et al., 2014). Response diversity is related to the diversity of taxa and ecological niches (Elmqvist et al., 2003). It is also related to genetic diversity and phenotypic plasticity, the ability of an organism to change its phenotype in response to changes in the environment, which may enable shifts in phenology and provide phenotypic variability under environmental changes – thus enhancing adaptability to climate change.

Resilience is also linked to spatial and temporal heterogeneity at different scales (Landis, 2017) (Table 2). Spatial heterogeneity is a result of variation in land-use/practices and environmental conditions. Temporal heterogeneity refers to variability in climate, water and soil conditions and in practices (e.g. crop rotation). Spatial and temporal heterogeneity contributes to the complexity of the system. System simplification that leads to weakening of cross-scale interactions is a symptom of the loss of resilience or the loss of the capacity to recover after disturbance.

While resilience theory provides a valuable framework for understanding dynamics in production systems, assessing and measuring social-ecological resilience are challenging, not least because of the multiple interacting factors that need to be taken into consideration. Measuring, assessing and monitoring with a narrow set of indicators may limit appreciation of the system dynamics needed to apply resilience thinking and inform management actions (Quinlan et al., 2016). In recent years, the increasing need to build resilience has led to efforts to develop tools for assessment, monitoring and quantitative measurement of resilience (Quinlan et al., 2016). There has been considerable progress in the field of resilience assessment in production systems (Cabell and Oelofse, 2012; Mijatovic et al., 2013; Bezner-Kerr, Sieglinde and Valerie, 2014; FSIN, 2014; FAO, 2015). Different components of BFA, and especially the diversity of varieties, breeds, crop species and land uses, have been recognized as important indicators of resilience (see for example Choptiany et al., 2015).

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4. Methodology

A search for case studies that link BFA and resilience was undertaken by screening case studies and reviews from the ScienceDirect, Scopus and Google Scholar databases. Peer-reviewed literature was complemented, where appropriate, with relevant working papers and project reports.2 Literature was screened initially with a broad set of search terms that were neither scale- nor sector-specific. Sector-specific searches were also undertaken to ensure adequate coverage of all components of BFA, including associated biodiversity (Table 3). Environmental-change terms were not included so as not to bias the search towards particular stresses and shocks. The search results were reviewed to determine which threats were overrepresented and which might represent research gaps.

The results, conclusions and recommendations of this thematic study are built upon the review of 507 papers, which include background literature on the various sectors and topics addressed as well as 238 individual case studies.

Selection and exclusion criteriaThe abstracts from case studies identified through keyword screening were reviewed. Case studies included in the analysis met the following criteria:

• they describe an aspect of environmental change;• they include a description of diversity (genetic, species or ecosystem); and• they address one or more ways in which biodiversity contributes to coping with or

managing environmental stress and change in production systems.Case studies were excluded using the following criteria:

• lack of adequate information on the link between stress, diversity and the resilience of the production system;

• lack of evidence of a contribution of BFA to resilience as described above or to resilience in production systems per se; and

• a concern with positive contributions of diversity to desirable human outcomes (food security, health, nutrition, income) that did not include an explicit consideration of resilience as described above.

2 The documents identified were used to create a BFA database, which was added to the existing REFARM resource maintained by Platform for Agrobiodiversity Research with the support of the CGIAR Research Program on Climate Change, Agriculture and Food Security (http://agrobiodiversityplatform.org/refarm). In the case of grey literature for which a reference was not available, a case study was included in the database and cited as the REFARM URL in the tables.

Table 3. Search terms used in screening literature on BFA and resilience

General search terms

Resilience terms “resilience”; “recovery”; “adapt*”; “restoration”; “stress”; “stability”

BFA terms “agrobiodiversity”; “genetic resources”; “biodiversity”; “agriculture”

Ecosystem-function terms “ecosystem service”; “functional diversity”; “response diversity”

Production-system terms “agroecosystem”; “production system”; “production environment”; “landscape”; “seascape”

Sector-specific search terms for BFA

Plants “crops”; “landraces”; “varieties”; “cultivars”

Trees “trees”; “forestry”; “agroforestry”; “provenance”

Animals “livestock”; “breeds”

Fisheries and aquaculture “fish”; “fisheries”; “marine”; “aquatic”; “freshwater”

Associated biodiversity “soil diversity”; “microbe”; “fungus”; “pollinator”; “pest”; “mangrove”; “reef”

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Case studies were included if the measured or described outcome was consistent with ecological characteristics of resilience (Table 2) and if information on the outcome was combined with information on BFA and on stress or sudden shocks. For instance, studies demonstrating yield stability over time in the face of abiotic stress were included, while those demonstrating increases in yield without mention of shock, stress or adaptation were not. This method for the selection of case studies accentuated some of the disparities between sectors, and highlighted the knowledge gaps that are discussed in the final section. Results from relevant ecological and experimental case studies with findings relevant to processes within production systems that support the provision of ecosystem services (e.g. soil properties and pest–predator dynamics) were also included. Additional studies were included at the recommendation of a panel of expert reviewers.

Two hundred and thirty-eight individual case studies met the criteria described above. Their findings on the relationship between BFA and resilience in relation to particular aspects of ecological resilience are summarized in Tables 4 to 20.

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5. Results

5.1. Genetic diversity 5.1.1. CropsGenetic diversity provides resilience by contributing to production stability and by enabling long-term adaptation. Production stability is a result of: (i) tolerance and resistance to biotic and abiotic stresses; and (ii) multiple services provided by genetic diversity, which may include pest and disease control and soil health (Balemie, 2011; Jarvis et al., 2011). Genetic diversity has been demonstrated to provide production stability and enable long-term adaptation in response to various shocks and stressors (Table 4) through a number of different mechanisms. Complementarity of traits and responses in a mixture, population or assemblage can increase overall stability. For instance, varietal mixtures of cowpeas with different seasonality stabilized production against mid-season drought (Hall, 2004). Response diversity is a means by which variability in organisms’ responses to environmental change is critical to a system’s resilience (Elmqvist et al., 2003). For instance, intercropping of varieties with varying water-use efficiencies stabilized yield in a drought-prone environment (Thiaw, Hall and Parker, 1993). Phenotypic plasticity (Bernhardt and Leslie, 2013) refers to the ability of a genotype to express more than one phenotype when exposed to different environments or alter its phenotype in response to changes in environmental conditions.

Adaptation to long-term environmental changes may reflect both phenotypic plasticity and continued evolution (Bellon, 2009). Maintaining evolutionary processes ensures the generation of new combinations of genes in response to stresses and climatic variability (Bellon et al., 2017). Genetic variants contributing to resilience are often found in traditional varieties or landraces and in the wild relatives of crops (Teshome, Brown and Hodgkin, 2001; Newton et al., 2010). However, while traditional varieties may perform better under stressed conditions, they can be lower yielding than improved cultivars under optimal conditions and this may limit their benefits to diversified farms if farmers choose to plant them in lower quantities (Ifejika-Speranza, Boniface and Wiesmann, 2008). Trade-offs between yield and resilience can be managed through practices that harness complementarity among physiological and phenological traits (e.g. architecture and seasonality) as well as specific resistances and tolerances.

Cultivation of varietal mixtures may confer enhanced resilience to biotic and abiotic stresses (Jarvis et al., 2011; Creissen, Jorgensen and Brown, 2016). One study examined the relationship between intraspecific diversity and yield in cultivar mixtures using a meta-analysis of 91 studies and more than 3 600 observations, and found that in cultivar mixtures with more functional-trait diversity yield increased by 2.2 percent overall in comparison to monoculture (Reiss and Drinkwater, 2017). This diversity effect was stronger, resulting in higher relative yields, under biotic stressors, such as disease pressure, and abiotic stressors, such as low levels of soil organic matter and nutrient availability (ibid). Cultivar mixtures also showed higher yield stability than monocultures, especially in response to annual weather variability over time (ibid).

Key practicesThe following practices emerged from the literature review as being of key importance in the contribution of genetic diversity to resilience in crop production.

On-farm conservation. On-farm conservation is an important strategy for maintaining genetic diversity as a source of stress tolerance and for maintaining evolutionary processes that ensure the generation of new combinations of genes in response to stresses and climatic variability. Stress-tolerance traits such as drought tolerance can be developed and maintained through continued “in situ” exposure (Kotschi, 2006). In marginal environments, maintaining

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Table 4. Contributions of genetic diversity to resilience in crops

Case study Shock or stress Reference(s)

In a period of prolonged drought stress in Mali and Niger, traditional varieties of sorghum and pearl millet showed an increased frequency of early flowering; a key early-flowering gene responsible nearly doubled in frequency in less than 20 years.

Drought Vigouroux et al., 2011

In dry districts of both Northern Karnataka and Andhra Pradesh, India, varieties of drought-adapted minor millets remained productive when all other crops failed due to extreme drought, playing an important role in food security for people and livestock. However, the arduous processing and low market returns associated with minor millets have limited their expansion.

Drought Bala Ravi, 2004; Fischer, Reddy and Rao, 2016

In Mediterranean climates, water stress at the end of barley life cycles threatens production. Studies of the effects of drought on yield in desert ecotypes of barley identified genomic regions associated with better performance under water stress.

Drought Comadran et al., 2008

In on-farm experimental trials in Yunnan province, China, glutinous rice and non-glutinous hybrid varieties with lower susceptibility to blast were planted in monocultures and mixtures. The mixtures showed reduced panicle blast severity, which averaged 20% and 2.3% in the glutinous and hybrid monocultures, and 1% in the mixture.

Pests and diseases Zhu et al., 2000

Increased diversity of varieties of bean, banana and plantain, measured both by number of varieties and evenness of their distribution, corresponded to a decrease in pest and disease damage, and a decrease in variance in pest damage. Some traditional varieties showed higher resistances than modern varieties across sites.

Pests and diseases Mulumba et al., 2012

Leaves of wild oat and barley showed less reduction in net photosynthetic rate and a slower rate of disease-associated senescence than cultivated genotypes of the same crops under comparable severities of powdery-mildew infection.

Pests and diseases Sabri, Dominy and Clarke, 1997; Akhkha, Clarke and Dominy, 2003

126 cultivars of six forage species were evaluated at multiple sites in Finland over a 30-year period for their response in terms of dry-mass yield to agroclimatic variability. Cultivar mixtures generally showed higher yield stability than monocultures, especially in response to annual weather variability at a site over time.

Weather variability Mäkinen et al., 2015

A field trial of three barley cultivars of varying resistance to barley mildew was planted in high-density mixtures and pure stands of different densities. Disease severity was reduced in the mixtures. In spite of the reduction in disease, mixtures yielded less than the mean of the pure stands at the same density.

Pests and diseases Finck et al., 1999

Disease was found to be less likely to spread between diversified wheat varieties possessing different specific resistances than between varieties possessing the same resistance.

Pests and diseases Priestley and Bayles, 1980

Genetic diversity of wheat varieties in Sicily can reduce variance in yield when pesticide applications are low, and high levels of diversity reduce the risk of crop failure by interfering with the evolution and proliferation of pest populations and reducing the extent of crop damage.

Pests and diseases Di Falco and Chavas, 2006

A meta-analysis of 91 studies and >3 600 observations found that mixtures with more cultivars and those with more functional-trait diversity gave higher relative yields when subjected to biotic stressors such as disease pressure and abiotic stressors such as low levels of soil organic matter and nutrient availability and annual weather variability

Biotic and abiotic stresses

Reiss and Drinkwater 2017

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adapted varieties through propagation can contribute to stability in crops (Jarvis et al., 2011). Large genotype by environment interactions for production traits found in genetically diverse crops such as cassava underscore the importance of maintaining and evaluating crops in the environments in which they evolved (Calle et al., 2005; Were et al., 2012). On-farm conservation is particularly important in centres of crop diversity rich in local varieties and crop wild relatives that can provide adaptive or other useful traits (Bellon and van Etten, 2014; Jarvis et al., 2011; Mercer and Perales, 2010).

Diversification. The use of a number of diverse varieties, particularly in mixtures, was identified as a strategy for managing biotic stresses (Finck and Wolfe, 1997; Zhu et al., 2000; Mulumba et al., 2012). Increasing diversity through mixtures of genetically diverse varieties can be an important way of coping with biotic and abiotic stresses, including high pest and disease pressure (Mulumba et al., 2012; Finck and Wolfe, 1997; Priestley and Bayles 1980) and recurrent drought and degradation (Di Falco and Chavas, 2006; Di Falco, Chavas and Smale, 2007). Intraspecific diversity was frequently found to stabilize production under adverse environmental conditions and weather variability (Prieto et al., 2015; Reiss and Drinkwater 2017).

Maintenance of seed systems and traditional knowledge. Maintaining and supporting seed-exchange systems, and associated traditional knowledge, that promote the access of farmers to a range of diverse varieties improves the resilience of production systems (Brush, 2004). In stress-prone and marginal production systems, the use of genetic resources may be strongly influenced by farmers’ traditional knowledge, preferences and practices, and social networks (Brush, 2000; Bellon, 2009; Labeyrie, Bernard and Leclerc, 2014). Informal seed-exchange systems are especially effective at maintaining high diversity, and participation in social networks has been demonstrated to facilitate access to genetic resources that can aid farmers in coping with crop failures, drought and environmental uncertainties (Pautasso et al., 2013).

Alternative approaches to breeding have been developed, some of which, such as participatory variety selection and participatory breeding, involve collaboration with farmers (Ceccarelli, 2009). Evolutionary breeding provides a framework for developing new varieties/populations while maintaining a high degree of genetic variation to allow for adaptability to fluctuations in environmental conditions (Döring et al., 2011; Murphy et al., 2016).

Ex situ conservation of crop genetic resources maintains genetic diversity than can be used in conventional and alternative approaches to breeding or can provide a source of germplasm that is pre-adapted to projected conditions under climate change (Jarvis et al., 2008b).

Accelerated breeding through genetics and genomics-assisted approaches. Genetic-mapping approaches, such as quantitative trait locus (QTL) mapping and

Case study Shock or stress Reference(s)

Varietal mixtures of winter barley were more tolerant of unexpected environmental stresses, with greater capacity to stabilize production.

Biotic and abiotic stresses

Creissen, Jorgensen and Brown, 2016

High levels of genetic diversity in wheat reduced yield variability in degraded and drought-affected areas in the Tigray region of Ethiopia.

Drought Di Falco, Chavas and Smale, 2007

Intercropping of cowpea varieties with complementary seasonality results in resilience against midseason droughts.

Drought Hall, 2004

Varietal intercropping in drought-prone environments results in higher or more stable yields and higher land equivalency ratios.

Drought Thiaw et al., 1993

In managed grasslands, temporal stability of production increased with the number of genotypes present under both drought and non-drought conditions.

Drought Prieto et al., 2015

Table 4 Cont'd

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Table 5. Contributions of genetic diversity to resilience in trees

Case study Shock or stress Reference(s)

Distribution of Prosopis africana seed from populations collected from drier regions of the semi-arid Sahel showed better growth and survival across regions and climates than provenances selected from regions with higher precipitation.

Drier climates Weber et al., 2008

In an approach called “composite provenancing”, plantations are established with a mix of germplasm from environmentally different sites and thinned as response to climate is demonstrated over the years.

Changing climate Bosselmann et al., 2008; Hubert and Cottrell, 2007

Populations of Pinus oocarpa from low altitudes in Mexico were found to have a slower growth rate associated with drought stress avoidance. Managers need to assist natural processes by transferring genotypes to higher elevations in anticipation of more-arid future conditions. Maps of moisture indices should be a priority in establishing seed zones for adapted material.

Drier climates Sáenz-Romero, Guzmán-Reyna and Rehfeldt, 2006

Pinus hartwegii and P. devoniana inhabit wide altitudinal ranges in montane Mexico, including up to the highest elevations of tree occurrence. The frost tolerance of seedlings decreased on average by 2–5% for every 100 m decline in the altitude of the source of the seed.

Frost damage Viveros-Viveros et al., 2008 ; Sáenz-Romero and Tapia-Olivares, 2008

There is evidence for natural selection of ozone tolerance in some varieties of Populus tremuloides, with some able to maintain higher fitness and survival under moderate and high ozone concentrations.

Ozone damage Karnosky et al., 2003; Berrang, Karnosky and Bennett, 1989

Populations of beech trees with the highest values of genetic diversity across multiple measures exhibited more stable growth rates when exposed to acute air pollution.

Pollution Müller-Starck, 1985; 1989

Genetic variability in disease response has helped to identify rare alleles that provide the basis of resistance against diseases such as chestnut blight, Dutch elm disease and ash dieback. These genes are being utilized in breeding programmes and conservation efforts.

Disease resistance Griffin, 2000; Yanchuk and Wheeler, 2008; McKinney et al., 2011; Diskin, Steiner and Hebard, 2006

Rootstocks influence grapevine resilience during and after drought, with certain combinations of rootstock and scion able to withstand drought and influence the resilience and recovery of the scion.

Drought recovery Sommer, Hancock and Downey, 2010; Whiting 2004.

In diseased and aging stands of cacao trees, those that were rehabilitated through grafting showed higher total fruit-set in spite of high levels of pest and diseases.

Pests and diseases Olaiya et al., 2006

In certain Norway spruce and European Scots pine provenances grown in heavy-metal contaminated soils, greater adaptive capacity was shown in individuals with higher heterozygosity.

Heavy-metal contamination

Bergmann and Hosius, 1996; Prus-Glowacki et al., 1999

Boreal forests are characterized by low species diversity but large population sizes with high intraspecific diversity that allows for high adaptive capacity. Traits involved in local adaptation to phenological and temperature gradients involve many genes of small effect.

Temperature and phenological change

Aitken et al., 2008; Gauthier et al., 2015

High on-farm genetic diversity in plantings of hybrid cacao trees managed by smallholders in Huallaga Valley in Peru facilitates participatory selection of improved clones adapted to their environment under low-input conditions.

Unique microclimate

Zhang et al., 2011

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genome-wide association studies, facilitate the discovery of candidate genes underlying adaptive traits (Scheben, Yuan and Edwards, 2016). Increased understanding of the physiological mechanisms and regulatory pathways underlying adaptive traits assists efforts to introgress useful traits in breeding programmes (e.g. identification of cold-tolerance genes in barley, heat-tolerance genes in bread wheat and candidate gene identification for drought tolerance in chickpea) (Scheben, Yuan and Edwards, 2016). In addition to specific resistances, mapping of traits related to the regulation of plant and root architecture can support breeding and development of resilient varieties (Uga et al., 2013). For example, increased expression of the enzyme cytokinin oxidase/dehydrogenase increased root biomass in tobacco and Arabidopsis, enhancing drought stress (Werner et al., 2010). When breeding for adaptive traits, phenotyping should be performed under suboptimal and multistress environments to realize the full genetic potential of the germplasm being evaluated (Kissoudis et al., 2016).

5.1.2. Forest and tree cropsTree populations have higher genetic diversity than populations of most other known organisms (Hamrick and Godt, 1989). The ability of trees to adapt to long-term changes and respond to shocks and perturbations, both through genetic responses and through phenotypic plasticity, is of great importance to the health of forest trees, which are stationary and long-lived, and are therefore subject to a wide range of climatic variations and extreme weather events (Schaberg et al., 2008; FAO, 2014). The same is true of trees outside forests, and is important for species that are used in agroforestry. Although it is difficult to predict the response of forest species to future anthropogenic or environmental changes (DeHayes et al., 2000), genetic diversity in tree populations has been demonstrated to maintain adaptive capacity (Thompson et al., 2009; Table 5). Phenotypic plasticity can play a critical role in helping trees to adapt quickly to a range of conditions (Thompson et al., 2009). Maintaining heterozygosity and co-dominant alleles (both alleles at a locus can be expressed) are potential mechanisms by which genetic diversity contributes to resilience in certain tree species, with cumulative exposure to multiple stressors over time favouring heterozygotes that can adapt to environmental variability (Schaberg et al., 2008). Average heterozygosity is lower across threatened taxa than in related non-threatened taxa, offering support to the theory that genetic diversity corresponds to an evolutionary advantage (Spielman, Brook and Frankham, 2004).

Appropriate management of genetic diversity in trees is important in ensuring that it contributes to resilience. Rare alleles can be a source of adaptive potential, but they may also be deleterious and persist at low frequencies in tree populations (Dawson et al., 2010). Shifts in the frequencies of rare genes in populations may arise as unintended consequences of management and may alter the adaptive capacity necessary for tree and forest health, while appropriate forest management can help to promote genetic fitness (Schaberg et al., 2008). For example, in silvicultural practices where regeneration of forestry species relies upon open pollination, care must be taken not to indirectly select against desirable phenotypes through harvesting and removal of the best genetic stock.

Adaptive introgression of alleles conferring resistance to specific pests and diseases can be a slow process in trees relative to crops with shorter generation cycles, but can be effective, as demonstrated by the hybridization and backcross breeding of the American chestnut with the Chinese chestnut (Diskin, Steiner and Hebard, 2006). Despite increased availability of genetic and genomic resources for different species, demonstrated progress in genomic-assisted breeding methods for climate resilience in tree and forest crops has been slow, owing to long generation intervals; however, the approach has potential to be an important strategy for increasing climate resilience (Kole et al., 2015).

In maintaining or planting trees on farms and across a landscape, there can be trade-offs between planting a number of different species and maximizing the genetic diversity within a single species. Identifying the genetic basis for resistance to a broad range of threats such as

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Table 6. Contributions of genetic diversity to resilience in livestock breeds

Case study Shock or stress Reference(s)

Zebu cattle breeds deal better with low-quality forage than taurine (Bos indicus vs Bos taurus), although taurine have better feed-conversion ratios when fed on high-quality feed.

Poor-quality feed Pilling and Hoffmann, 2015

Heat tolerance and water requirements vary between breeds; for Bos indicus, water intake increases from 3 kg/kg dry matter at 10 °C to 10 kg/kg at 35 °C, for Bostaurus, intake increases from 3 kg/kg to 14 kg/kg.

Heat stress McDowell, 1972; Pilling and Hoffmann, 2015

Tropical cattle breeds have better heat tolerance than temperate-zone breeds, linked with skin and hair properties, sweating and respiration, tissue insulation, surface area relative to weight or lung size, endocrinological profiles and metabolic heat production.

Heat stress Thornton et al., 2009

Local livestock breeds have lower food-intake requirements, making them well suited for smallholder systems.

Poor-quality feed McDowell, 1972

Heat tolerance in chickens varies between breeds based on feather characteristics; “naked-neck” and “frizzle-feathered” chickens are better able to cope with high temperatures.

Heat stress Horst, 1988

Dryland breeds are often better able to cope with water shortages and graze over wider areas.

Water stress Pilling and Hoffman, 2015

Genetically diverse village chickens in Africa are better adapted than commercial lines to brooding and chick rearing in low-nutrition conditions.

Poor-quality feed Leroy et al., 2012

In Lesotho, indigenous cattle breeds have proven to be highly adapted to drought, low temperature and snowfall.

Drought and cold Dejene et al., 2011

A genetic basis for resistance to a range of parasites and diseases, including fungi, protozoa, worms and tick-borne diseases, has been identified in many breeds of sheep and cattle.

Pests and diseases Bishop et al., eds, 2010; FAO, 2009; Burke and Miller, 2008; Goldberg, Ciappesoni and Aguilar, 2012; Conington et al., 2008; Glass and Jensen, 2007; Kemper et al., 2011, Mapholi et al., 2014

Neuquén Criollo goats are small, hardy animals raised under cold, semi-arid conditions in a transhumance system in the Argentine province of Neuquén. The breed is selected for hardiness, herding behaviour, good parentage and disease resistance. Because of their high nutritional requirements and lack of hardiness, exotic goats such as angoras do not thrive in the local production system.

Drought and cold Lanari, Pérez Centeno and Domingo, 2007

pests and disease and drought tolerance is a high priority in the breeding and domestication of trees (Yanchuk and Wheeler, 2008). Improved understanding of the molecular basis for adaptation in tree crops is an important area for further development – less than 8 percent of species identified by countries as priority species had been characterized genetically as of 2014 (FAO, 2014), although this is rapidly changing with the increased availability and affordability of sequencing technologies (Batley and Edwards, 2016).

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Key practicesThe domestication, improvement and selection of new tree crops. Tree selection efforts, including agroforestry practices on farms, can facilitate ongoing evolution and in situ conservation of important adaptive germplasm while also improving food security (Ofori et al., 2014). The selection and improvement of high-value tree crops in agricultural landscapes makes an important contribution to rural livelihoods while allowing for participatory selection of locally suited genotypes (ibid). Community nurseries and genebanks play an important role in maintaining diversity, selecting for locally adapted varieties, and maintaining access to diverse, locally adapted and improved germplasm for breeding, production and restoration.

In situ conservation and agroforestry. Maintaining the genetic diversity of trees on farms and across landscapes provides resilience and stability. This can include maintaining existing trees as sources of genetic variation adapted to local conditions. It is important to modify harvesting practices to ensure that trees that are well adapted to a particular site are not all removed and can continue to contribute to seed production (Schaberg et al., 2008). Maintaining connectivity by reducing fragmentation is important in ensuring that gene flow can occur (Thompson et al., 2009). Tree species can be managed for genetic diversity through farmer seed exchange, pollination management and conservation in agroforestry systems and managed forests (Dawson et al., 2010).

Planting adapted varieties. Planting germplasm that is pre-adapted to a broad range of environmental conditions or that has ecological tolerances matched to projected future climates can enhance adaptive capacity and evolutionary potential in tree populations (Sáenz-Romero, Guzmán-Reyna and Rehfeldt, 2006; Weber et al., 2008; Dawson et al., 2010). Various related strategies relying upon this principle have been suggested, including assisted migration, composite or predictive provenancing and genetic translocation, and illustrate the importance of preventative rather than responsive measures in ensuring climate resilience in long-lived perennial species (Thompson et al., 2009; Sgrò, Lowe and Hoffmann, 2011).

Grafting. The use of genetically different rootstocks and interstocks can enhance resilience by conferring tolerance of, or resistance to, soil-borne diseases, changing tree architecture and allowing adaptation to local abiotic stresses such as salinity or drought (Warschefsky et al., 2016). Grafting increases the efficiency of adaptations by combining the favourable traits of a productive scion with the benefits of locally adapted rootstock, and has been reported in at least 70 different tree species (Warschefsky et al., 2016). Furthermore, rehabilitation grafting onto seedlings or onto adventitious shoots following coppicing can be a rapid way to introduce improved or adapted varieties to a farm or orchard and to promote recovery following disturbance or degradation (Are and Jacob, 1970; Olaiya et al., 2006; Adebiyi and Okunlola, 2013).

5.1.3. LivestockMechanisms by which genetic diversity in livestock contributes to resilience include the use of local breeds. Many breeds have adaptations to stress-prone environments, including to climatic stressors (Tempelman and Cardellino, eds, 2007). They have also often been demonstrated to be resistant to specific pests and diseases that afflict exotic breeds if they are kept in the same locations (Bishop et al., eds, 2010; FAO, 2009; Burke and Miller, 2008; Goldberg, Ciappesoni and Aguilar, 2012; Conington et al., 2008; Glass and Jensen, 2007; Kemper et al., 2011; Mapholi et al., 2014). In marginal environments with poor-quality fodder and limited water, locally adapted breeds are often more effective than improved breeds (Lanari, Pérez Centeno and Domingo, 2007; Leroy et al., 2012).

There are differences among breeds in physiological responses and thermoregulatory control that underlie tolerances (Hoffman, 2010; Hall, 2004; McManus et al., 2008). Homeostatic regulation determining the mobilization of body reserves and nutrient partitioning under stresses, such as those associated with underfeeding and reproduction, also differs across breeds and affects aspects of resilience, including adaptability and recovery (Friggens et al., 2013). Increased nutrient partitioning towards production and away from other functions

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can negatively affect reproductive or health traits, a trade-off with implications for resilience (Douhard, 2013). While selection for milk yield in dairy cattle has increased production in favourable environments, the resulting genotypes can have decreased survival and fecundity under stress (Pryce et al., 1997; King et al., 2006). Similarly, productivity gains in cattle growth rates and leanness in pigs and poultry have corresponded with a decline in heat tolerance (Zumbach et al., 2008; Dikmen and Hansen, 2009). The capacity of most livestock breeds to cope with increased frequency of heat stress is not well known. For example, it is uncertain whether cattle breeds will be able to tolerate the mean temperature increases predicted for the coming decades, particularly in the tropics (Thornton et al., 2009). Immune response suppression following heightened exposure to UVB radiation as a result of ozone depletion has been demonstrated in mammalian cellular responses (Baylis and Githeko, 2006). Interactions among multiple stressors are difficult to predict as the genetic basis of adaptation traits is often not well defined.

Genomic research has improved understanding of the regulation of stress in different breeds and revealed genes, and signatures of selection associated with resistance in different breeds (Misztal and Legarra, 2017; Elbeltagy, 2017; Kim et al., 2016). These include adaptations that affect water use and heat stress in Bactrian camels, sheep, goats and chickens (Rothschild and Plastow, 2014).

Genotype by environment interactions affect trait expression across environments (Simm, 1998; Douhard, 2013). A landscape genomics approach, in which populations and breeds from different geographic regions are analysed and compared, is recommended as a way of improving understanding of the genetic basis of the adaptation of genotype to environment (Seré et al., 2008; Thornton et al., 2009; Rothschild and Plastow, 2014).

Key practicesUse of locally adapted breeds, particularly in marginal environments and smallholder and pastoralist production systems with limited access to inputs. Locally adapted breeds can also be used in breeding programmes to contribute genes that improve resistance to biotic and abiotic stress in newly developed breeds or they can be maintained as pure-bred populations for use in appropriately designed crossing schemes that provide an ongoing supply of cross-bred offspring in which local adaptations are combined with other desirable traits. In the context of climate change, shifting to the use of breeds that are well adapted to altered local climates is an option. However, more information is needed on the adaptive characteristics of specific breeds and their performance across multiple environments (Pilling and Hoffman, 2015).

Better characterization of indigenous breeds and improved understanding of adaptation using an approach that considers genetic data as well as local knowledge and production-system features including socio-economic information and environmental data (climate, soil, vegetation and water resources) (Boettcher et al., 2014; Hoffmann, 2010).

Approaches including genomic selection and marker-assisted selection can enhance understanding of the genetic regulation of physiological responses and enable prediction of genotype by environment effects (Boichard, Ducrocq and Croiseau, 2016). Genotyping is cheaper than progeny testing and has quickly become accessible even to midsize and smaller breeding operations (Boichard, Ducrocq and Croiseau, 2016). Increasingly, genomic tools are being used to address the challenges of smallholder production including environmental change (Rothschild and Plastow, 2014).

5.1.4. Aquatic organismsGenetic diversity contributes to resilience in aquatic species in various ways, in particular with regard to variability in tolerance to stresses, including abiotic stresses such as changes in temperature and salinity and biotic stresses such as parasites (Table 7). Different genetic strains may vary in quantitative traits such as growth and tolerance to certain stressors, which can be selected for through domestication programmes.

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Information on the genetic diversity of aquatic invertebrates important to food and agriculture is limited (Pullin and White, 2011). The species that have been assessed have high levels of genetic diversity, particularly heterozygosity (Pullin and White, 2011), although it has been suggested that high levels of diversity (i.e. heterozygosity) in marine species such as molluscs could in fact reflect cryptic species (morphologically indistinguishable species), rather than different within-species populations (Thorpe, Solé-Cava and Watts, 2000). Morbidity and mortality in fish, both in the wild and in aquaculture, are governed by multiple interacting factors. The interplay of genetic and environmental factors with phenotypic plasticity in governing aquatic organisms’ responses to and recovery from shocks is still poorly understood (Pullin and White, 2011). Traits important for adaptation and survival in aquatic species include fecundity, tolerance of low water quality, disease resistance, growth and feed conversion (Pullin and White, 2011). However, little is known about some of the key traits influencing resilience, for instance the genetic basis for tolerance of turbidity and siltation in aquatic species (Pullin and White, 2011). Thermal tolerances have been found to be heritable in a wide range of aquatic organisms, but are difficult to measure experimentally because of confounding effects of other stresses. For instance, tolerance may be lowered by handling, sublethal levels of ammonia or poor nutritional status (Linton et al., 1998).

Key practicesBreeding and domestication drawing upon variability within species with regard to traits of interest. Heritable traits that improve stress tolerance, resistance and recovery from shocks can potentially lead to rapid adaptation in aquatic species, as high fecundity in wild populations and in hatcheries permits natural selection to produce adapted strains in a few generations (Pullin and White, 2011). A number of QTLs for important traits have been

Table 7. Contributions of genetic diversity to resilience in aquatic organisms

Case study Shock or stress Reference(s)

126 genotypes were counted within a Baltic population of eelgrass, which varied in their responses to heat waves from a three-fold increase in shoot density to inability to recover from a 50% loss in shoot density.

Heat shock Reusch et al., 2005

The thermal tolerance of a northern population of striped bass (Morone saxatilis) is generally broader than that of southern populations.

Heat stress Molony, Church and Maguire, 2004

Domesticated rainbow trout in Western Australia are better adapted to high temperature than a naturalized line in terms of survival and weight gain.

Heat stress Molony, Church and Maguire, 2004

Wild strains of brown trout, brook trout and rainbow trout had critical thermal maxima that exceeded those of domesticated strains by 0.5–1.6 °C.

Heat stress Carline and Machung, 2001

The channel catfish (Ictalurus punctatus) responds to low temperatures by adjusting the expression of many genes.

Cold stress Ju, 2002

Cold tolerance in red drum (Sciaenops ocellatus) is highly heritable.

Cold stress Pullin and White, 2011

Oreochromis mossambicus, possibly the species of tilapia that is most eurythermal and euryhaline, is important as a source of genetic material for the development of salt-tolerant hybrids.

Salinity Pullin and White, 2011

Breeding of salinity resistant aquaculture species is a priority in the face of rising sea levels.

Salinity De Young et al., 2012

Resistance of some wild salmonids to microbial diseases and parasites demonstrates the importance of wild relatives in breeding programmes for farmed fish.

Pests and diseases Withler and Evelyn, 1990; Pullin and White, 2011

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legumes is below-ground niche complementarity via interspecific root stratification coupled with modified nodulation patterns (Bargaz et al., 2015, 2016).

Planting appropriate species for integrated pest management (IPM), including promoting or tolerating wild species within and around fields, can reduce the incidence of pest damage (Letourneau et al., 2011). IPM strategies are most effective when they combine

Table 8. Contributions of species diversity to resilience in crops

Case study Shock or stress Reference(s)

Intercrops, hedgerows and cover crops, particularly those using nitrogen-fixing species, can maintain production over years in water-stressed environments with poor soil fertility.

Drought stress; poor fertility

Buckles, Triomphe and Sain, 1998; Rao and Mathuva, 2000; Diop, 2000; Bezner-Kerr, Sieglinde and Valerie, 2014; Bunch, 2000; Kaumbutho and Kienzle, 2007

The integration of native vegetation, particularly grasses, into cropping systems can help to stabilize soils and retain moisture as mulch, as well as to buffer the effects of erosion, drought and soil moisture-related stresses.

Erosion; water stress; drought

Dey and Sarker, 2011

In South Africa, biennial wild rooibos showed greater resilience to drought than annual rooibos and was harvested to buffer losses in rooibos production.

Drought Archer et al., 2008.

Increased water-use efficiency of mixed cropping has been demonstrated under experimental conditions with intercrops of sorghum, peanut and millet, with all crops consistently out yielding monocrops at five levels of moisture availability.

Drought Liu, Golding and Gong, 2008; Natarajan and Willey, 1986

Tithonia, a wild sunflower that grows in hedgerows and along roadsides in subhumid Africa, is used as a green manure. This has a positive impact on yields of maize and vegetables in areas with nutrient-poor soils. Tithonia contains high concentrations of nitrogen, phosphorus and potassium.

Degraded soils Sanchez, 2000

Intercropping of leguminous species improves both yield and yield stability in degraded soils.

Degraded soils Kang, Wilson and Sipkens, 1981; Rao and Mathuva, 2000

Crop diversification, including rotation and intercropping of crops with IPM species, is effective in reducing damage from pests and weeds.

Pest and weed invasion

Altieri, 1999; Sanderson et al., 2007; Kang, Wilson and Sipkens, 1981; Kahn et al., 1997; Chabi-Olaye et al., 2007; Pretty, 1999; Corre-Hellou et al., 2011

In southern Cameroon, the average yield loss due to borers was five times higher in a maize–maize sequence than in cover crop–maize sequences.

Pests and diseases Chabi-Olaye et al., 2007

Crop rotations help to reduce damage from pests. Pests and diseases Di Falco, Bezabih and Yesuf, 2010; Alam et al., 2012

Diversified cropping systems provide insurance against adverse weather events when the different crops exhibit different responses.

Weather extremes Alayón-Gamboa and Ku-Vera, 2011; Di Falco, Bezabih and Yesuf 2010; Adger et al., 2003; Di Falco and Chavas, 2009

Farmers faced with progressive flooding and droughts plant off-season crops to stabilize production during the year and provide security in months between primary crop production.

Flooding and drought

Chidanti-Malunga, 2011

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identified in aquaculture species including Pacific oyster, salmonids, channel catfish and Nile tilapia. These include temperature tolerance, growth and disease resistance (FAO, 2008).

Conservation of edge populations. Populations at the extremes of their ranges (thermal ranges, etc.) are more likely to have adapted to environmental extremes and may represent a source of adaptive traits; they may also be more vulnerable to fishing pressures owing to their greater exposure to stress. Their conservation can be prioritized to maintain adaptability and evolutionary potential (Brander, 2010).

Ex situ gene banking. Sperm cryopreservation and gene banking of live fish can help to ensure that genetic diversity important for resilience is conserved, and can facilitate the development of breeding programmes for fish species (Viveiros and Godinho, 2009).

5.2. Species diversity, including farming-system diversity 5.2.1. Crop species mixturesTraditional farming systems based on intercropping and crop rotation are known to reduce risks associated with fluctuation in market and agroclimatic conditions (Isaacs et al., 2016; Isbell et al., 2015). Various types of intercropping and crop rotation, along with the introduction of new crops, are effective approaches to improving resilience in production systems (Natarajan and Willey, 1986; Archer et al., 2008; Lin, 2011; Himanen et al., 2016). Diversification of fields with underutilized or neglected crops can improve resilience and help to meet other production objectives (Kahane et al., 2013). Crop diversification was shown to help improve resilience by enhancing suppression of pest and disease outbreaks, as well as by buffering crop production from climate variability, drought and extreme events (Table 8).

Crop-production strategies that diversify with non-crop species also provide important contributions to resilience, including through pest and disease management (Chabi-Olaye et al., 2007; Pretty, 1999) and the use of non-crop species to improve moisture retention (Dey and Sarker, 2011). There can, however, be trade-offs between yield and stability in diversified crop mixtures. Appropriate intercropping systems applying appropriate selection of species can help to strike a balance between farm-level productivity, resilience and environmental health (Delaquis, de Haan and Wyckhuys, 2018; Bantilan and Anupama, 2006; Makate et al., 2016). Perceptions of risk can play a significant role in determining a farmer’s course of action, as diversification may stabilize yields but may also reduce them overall (Ballivian and Sickles, 1994; Trenbath, 1999). Asset wealth, field size, access to information, exposure to agricultural extension officers and environmental conditions are among the factors determining the likelihood of crop diversification among smallholders (Bantilan and Anupama, 2006; McCord et al., 2015).

Key practicesDiversification using crop species mixtures, including intercrops, cover crops and crop rotations, can contribute to resilience (Lin, 2011). Diversification with indigenous crops and crop wild relatives stabilizes production during stressful climate and weather events, such as droughts, in marginal environments (Archer et al., 2008). Mixtures are most beneficial when response diversity is maximized (Trenbath, 1999). Benefits come from complementarity in water use, light interception and nutrient uptake (Natarajan and Willey, 1986; Liu Golding and Gong, 2008; Malézieux, 2012), microclimate regulation by the standing biomass of living crops of different statures, or soil enrichment and moisture retention by crop residues (Sanchez, 2000; Kaizzi, Ssali and Vlek, 2006; Lithourgidis et al., 2011; Rusinamhodzi et al., 2012).

Intercropping with annual and perennial leguminous species was shown to improve yield stability and productivity, minimize the need for inputs and replenish degraded soils (Kang, Wilson and Sipkens, 1981; Rao and Mathuva, 2000; Davis et al., 2012; Isaacs et al., 2016). One important mechanism for coping with water stress in intercrops with

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Table 9. Contributions of species diversity to resilience in agroforestry systems and mixed-species plantations

Case study Shock or stress Reference(s)

Following Hurricane Ike, diversified farms suffered 50% crop losses, as opposed to 90–100% in neighbouring monocultures; farms managed in accordance with agroecological principles showed faster recovery of productivity than monoculture farms, with 80–90% of productivity restored within 40 days of the hurricane.

Hurricane damage Machin-Sosa et al., 2010;

Tree-based systems were less affected than rice and rainfed-crop systems following extreme drought and flood; some tree species demonstrated better performance under harsh local climatic conditions and show potential to be managed for multiple benefits including resilience and adaptation to climate change.

Extreme drought and flood

Nguyen et al., 2013

Traditional agroforestry systems in which crops are planted beneath trees and fertilized with tree trimmings are better protected from soil erosion and more resilient against hurricane damage than non-agroforestry cropping systems in neighbouring communities.

Hurricane damage; soil erosion

Holt-Giménez, 2002

Under irregular temperatures and microclimate variability, agroforestry led to an increase in soil moisture and the best growing conditions for crops.

Climate variability

Lin, 2007

Diversified agroforestry systems mitigate temperature variations and stabilize local climate through shading, increased transpiration and reducing incident solar radiation.

Climate variability

Mbow et al., 2014

Tree–crop systems enhance the suitability of degraded sites for crop production through improved water infiltration, regulation of microclimates and improved soil fertility, especially with the planting of nitrogen-fixing species.

Soil degradation Montagnini and Nair, 2012; Altieri, 1999; Van Asten et al., 2011; Kwesiga and Coe, 1994

Species diversity in plantations corresponded with higher production and volume of spores from arbuscular mycorrhizal fungi, assisting with adaptation to nitrogen-limited soils.

Soil degradation Burrows and Pfleger, 2002

Greater resource-use complementarity in mixed-species plantations, based on structure, guilds and growth rates, light and shade requirements, and fungal associations, allows for more complete utilization of scarce soil nutrients.

Soil degradation Petit and Montagnini, 2006; Kelty, 2006

Planting of nitrogen-fixing leguminous trees in Southern Africa helped to stabilize crop production during drought and extreme weather events.

Drought Sileshi et al., 2012

Mixed-species plantations suffered less pest damage, due to reduced accessibility of host trees to pests, greater impact of natural enemies and diversion of pests.

Pests and diseases Kelty, 2006; Jactel, Brockerhoff and Duelli, 2005;

The response of mixed-species stands to abiotic stresses (drought, fire and wind) may be greater than monocultures if more-resistant species are planted, but can also increase vulnerability if less-resistant species are planted.

Drought, fire and wind

Bauhus et al., 2017

In most cases reviewed, tree diversity can reduce the incidence of specialist pathogens, but there is little evidence that tree diversity leads to positive effects in the presence of generalist pathogens.

Pests and diseases Bauhus et al., 2017

In a study of 208 forest plots across Europe, pest damage to broadleaf species significantly decreased with the number of tree species in mature forests, irrespective of climate.

Pests and diseases Guyot et al., 2016

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top-down and bottom-up controls through a large number of weak interactions; effective design of diversification strategies for IPM requires a comprehensive understanding of the underlying trophic relationships (Ratnadass et al., 2012).

Use of native plants in a production system provides diverse benefits and requires few additional resources. Benefits include adding biomass for moisture retention or structure (hedgerows, wild grasses that prevent erosion) and providing forage resources (Dey and Sarker, 2011; Diop, 2000; Bezner-Kerr, Sieglinde and Valerie, 2014).

5.2.2. Agroforestry and mixed species forests and plantationsAgroforestry offers multiple benefits to producers while often strengthening the system’s ability to cope with adverse impacts of shocks and environmental uncertainty (Table 9). Heightened recovery from extreme weather events has been demonstrated repeatedly in agroforestry systems (Altieri, 2002; Holt-Giménez, 2002; Machin-Sosa et al., 2010). High-value products from diversified agroforestry systems may generate financial capital beyond subsistence levels alone, thereby aiding capital accumulation and re-investment at the farm level (Mbow et al., 2014).

In understanding the contributions of agroforestry systems to resilience, there is a need to differentiate between simple agroforestry systems (such as alley cropping, intercropping and hedgerow systems), annual crop–tree combinations, perennial tree–crop combinations and complex multistrata agroforestry systems that function like natural forest ecosystems but are integrated into agricultural management systems (Montagnini and Nair, 2012; Mbow et al., 2014).

Key practicesSelection of appropriate species. Species selection is important in maximizing the benefits from plantation mixtures. Certain tree species demonstrated better adaptive capacity under harsh local climate conditions and have potential to be managed for multiple benefits, while inappropriate combinations of species can increase vulnerability to abiotic stresses such as fires and drought (Nguyen et al., 2013; Bauhus et al., 2017). Trees can be selected to maximize particular functions in agroforestry systems, including nitrogen inputs from the litter of leguminous species, shade provisioning and prevention of soil erosion (Holt-Giménez, 2002).

Mixed crop–agroforestry combinations. Relevant approaches improve and stabilize the production of different components and confer structural and environmental improvements that enable the system to withstand shocks such as severe weather events or degradation due to soil erosion (Machin-Sosa et al., 2010; Sileshi, Debusho and Akinnifesi, 2012).

5.2.3. Species diversity in livestockMost of the traits described in Section 5.1.3 also apply to livestock species diversity (i.e. differences in disease tolerances, nutrient partitioning, behaviour and products). There has been limited work on direct impacts of climate change on heat stress in animals, especially in the tropics and subtropics (Thornton et al., 2009), and there are few physiological models relating climate to animal physiology (Easterling and Apps, 2005). The studies provided little information on the contribution of species diversity in livestock to resilience, but a few cases are noted in Table 10.

Key practicesDiversification at the species level can contribute positively to resilience, particular where complementarity in functional and response diversity is enhanced between species. Differences in feeding habits, water requirements and nutrient partitioning can allow animals to utilize a wide range of feed resources in the same area. For example, different ruminant and camelid species tend to utilize different types of vegetation.

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Substitutions. Replacement of heat and drought stress-prone species with more tolerant and adapted species can improve livelihoods and resilience.

5.2.4. Integrated crop–livestock systemsIntegration of livestock with cropping activities improves resilience at the field and farm scale, in particular by improving tolerance to stress, often by ameliorating the impacts of poor soil structure and low nutritional content, regulating the microclimate (Sanderson et al., 2013; Gil et al., 2017) and providing smallholders with a form of self-insurance against shock-related losses. Integrated crop and livestock systems were often associated with enhancements to ecosystem services, as animals provide a source of traction and may improve soil structure, and crop residues and organic manure improve soil composition (Table 11).

Key practicesComplementarity in resource use. By-products of one component of the system can serve as inputs elsewhere in the system. For instance, crops benefit from the input of organic manure, and livestock production is enhanced by the availability of nutritious forage and other feeds (Bonaudo et al., 2014; Thiaw, Hall and Parker, 1993; Akbar et al., 2000). Certain types of diversified system are encountered frequently, for example integration of livestock with a fodder or forage intercrop (Bonaudo et al., 2014; Thiaw, Hall and Parker, 1993; Akbar et al., 2000). The effectiveness of integrated systems depends highly upon crops and animals being combined in a complementarity manner that results in increased total productivity and enhanced resilience (Devendra, 2007).

Diversification, particularly into higher-value products and industries can benefit smallholders through higher returns and benefits to production, but may also increase vulnerability if high-value agricultural commodities are susceptible to stresses and shocks. Planned diversification with species that can enhance the nutrition of another component in a highly diversified system can greatly extend the benefits of diversification to resilience (Retama-Flores et al., 2012).

5.2.5. Integrated and multitrophic aquacultureIntegration of crops, livestock, trees and fish on farms can result in highly productive and complementary systems that are resilient to shocks such as drought and flooding and have distinct benefits to food security, nutrition and sustainable rural livelihoods (Table 12). Enhanced resilience of integrated and multitrophic aquaculture is primarily achieved in the following ways: complementarity of resource use by crops and fish, with highly integrated farms also making use of organic manure from livestock to enhance fish production; pest control through integration of multiple components, for example fish and ducks in flooded

Table 10. Contributions of species diversity to resilience in livestock

Case study Shock or stress Reference(s)

Species mixtures, or appropriately selected species, will be better suited to utilizing limited resources in stressed environments. Goats and camels make use of low-quality browse (shrubs and trees) more often than sheep and cattle.

Poor-quality feed and environmental uncertainty

Blench, 1999

Goats maintain their feed intake and digestion better than other livestock species under high temperatures and water shortages.

Temperature and water stress

Silanikove, 1997

South American camelids are better adapted than cattle to Andean regions as they are unaffected by altitude sickness. They also bite off forage plants rather than tearing them out, thus causing less damage to grasslands. Camelids are also more efficient than other species in digesting poorer-quality forage that is high in lignin.

High altitude conditions; poor-quality feed

Rodríguez and Quispe, 2007

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rice fields (Rashid, 2001; Liang et al., 2012); landscape engineering in the form of integrated farming and excreta/wastewater-fed aquaculture, such as paddy–reed–fish systems, that make the most of locally available nutrients (Ma, Liu and Wang, 1993); buffering against shock, as ponds on farms can help to mitigate drought, flood and food insecurity; and provision of ecosystem services, such as enhancing nutrient cycling, microclimate modification and carbon sequestration, at farm and landscapes scale.

Key practicesDiversification into high-value combinations and products, such as vegetables and fish that also have high nutritional content provides benefits for income diversification and food security at the household level.

Integration of ponds on farms stabilizes production and buffers against shocks in both drought-prone and flood-prone climates by providing drainage from the fields and water storage for dry periods. During droughts, households have depended upon ponds as a form of irrigation for crops and as a means of ensuring food security and providing substantial

Table 11. Contributions of species diversity to resilience in integrated crop–livestock systems

Case study Shock or stress Reference(s)

In Brittany, France, grazing in integrated crop–livestock systems is managed by dividing grassland into two plots, a dedicated grazing area and a security pasture for times when grass production is less predictable, helping to stabilize production.

Environmental uncertainty

Bonaudo et al., 2014

Livestock and grass intercrops have helped to restore the natural capacity of farmland over time, while fattening the animals with grass from the intercrops improves farm yields and income.

Degradation Thiaw, Hall and Parker, 1993

In the southeastern United States of America, winter forage cover crops provide a viable short-rotation opportunity following summer cash crops. Grazing by livestock rather than chemical termination maintained soil nutrients, while high surface-soil organic-matter-content resisted soil compaction. Cattle gain from feeding on the cover crop increased income.

Soil erosion; soil compaction

Sulc and Franzluebbers, 2014

In Cuba, diversified farms were found to be more productive, more energy-efficient and to manage nutrients better than farms specializing in a single product or crop, especially under conditions of low inputs and high uncertainty. Higher diversity contributed to reducing risk while increasing productivity.

Environmental uncertainty

Rosset et al., 2011

In Lesotho, farmers adapt diversification practices according to the terrain in order to manage pests and drought-related risks at different elevations. Upland farmers tend to grow a greater variety of crops in more equal proportions, whereas lowland farmers are more likely to mix livestock and crop farming.

Pests and drought Dejene et al., 2011

In the Sekyedumase district of Ghana, farmers adapt to increasing temperatures and water deficiencies by planting early-maturing crops, increasing the number of fruit and vegetable crops and diversifying into activities such as beekeeping, snail raising and plant nurseries.

Temperature stress; water stress

Fosu-Mensha, Vlek and MacCarthy, 2012

The fodder legume Lathyrus sativus is produced in rice fields to buffer shortages of fodder for dairy cattle, as well as to improve soil fertility.

Soil infertility and environmental uncertainty

Akbar et al., 2000

Animal traction on degraded farmland with poor infiltration increases stability and allows recovery of crop production.

Degradation Sanders, Nagy and Ramaswamy, 1990

Livestock serve as self-insurance for other on-farm activities, providing protection against shocks.

Environmental uncertainty

Berkvens, 1997; Abdulai and CroleRees, 2001

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profits (Karim et al., 2011; Brummett and Noble, 1995; Brummett and Chikafumbwa, 1995). Integrated aquaponics systems, such as floating vegetable gardens, are able to produce high-value crops continuously, particularly if organic manure is applied (Armillas, 1971; Irfanullah, Kalam Azad and Wahed, 2011).

Appropriate selection of species in highly diversified systems is critical to ensuring that integrated multispecies farming systems are more efficient and properly utilize complementarity between their components. It is important to consider the functional and lifecycle traits of the species used in diversification practices. For instance, farming of fish species with short generation intervals and short production cycles is likely to have the advantage of minimizing exposure to risks (Pullin and White, 2011).

5.3. Diversity at the landscape/seascape scaleIn this section, we review strategies in which the spatial or abiotic elements of a landscape or seascape confer, or contribute to, resilience in agroecological systems. This may include the spreading of risk across multiple locations, utilization of landscape and seascape complexity, and the modification or management of abiotic features of a landscape or seascape for enhanced resilience.

5.3.1. Spatial diversification of crops across a landscapeSpatial diversification of crops at a landscape scale may include specific pairings of crop traits at the genetic or species level, for example planting of particular varieties or species at different elevations, while in other cases the mechanisms may be more generic, such as a landscape modification that improves the suitability of an area for cropping. Frequently, the diversification of crops and cropping systems included the incorporation of non-crop plants such as hedgerows and field margins.

Diversification of cropping systems across landscapes is important in enhancing resilience (Reidsma and Ewert, 2008; Abson, Fraser and Benton, 2013), especially in highly dynamic production environments, such as those at high elevations, and resource-poor environments,

Table 12. Contributions of species diversity to resilience in integrated aquaculture systems

Case study Shock or stress Reference(s)

Aquatic and aquaponic systems based on traditional floating-farming systems in flood-prone areas utilize floating vegetation to cultivate vegetables in multiple, year-round cropping; such systems also support the production of high-value, short-rotation crops along river banks following floods.

Flooding Armillas, 1971; Irfanullah, Kalam Azad and Wahed, 2011

Ponds on farms can provide temperature-regulating services, mitigating the local impacts of both frosts and heat waves.

Temperature regulation

Musa, Allison and Ellis, n.d.

Seasonal aquaculture and fisheries in savannah and dryland ecosystems are precious resources as “wetlands in drylands”; small carp, catfish, tilapia and miscellaneous indigenous species can be farmed in cycles of as little as three months in areas where water supplies are uncertain.

Drought and water uncertainty

Karim et al., 2011; Brummett and Noble, 1995; Brummett and Chikafumbwa, 1995

The widespread adoption of integrated aquaculture can reduce soil erosion in the local environment.

Soil erosion IAASTD, 2009

Fish provide an IPM strategy in rice paddies; they support rice production by feeding on insect pests, improving oxygen circulation and adding fertilization.

Pests and diseases Rashid, 2001

Various methods of fish–duck farming can be effective at reducing pest and diseases; a “mixed pasturing” approach, utilizing multiple age classes of ducklings, was the most effective at reducing rice paddy hopper incidence and controlling weeds.

Weeds; pests and diseases

Liang et al., 2012

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such as drylands (Table 13). The benefits of stratifying production across spatial scales included buffering overall production against loss at any one elevation or in any one field, efficient utilization of limited resources such as water and nutrients, and use of landscape features for ecosystem services such as climate moderation, erosion protection and water provisioning. Manipulation of biophysical features of the landscape may further enhance adaptation to extreme and inhospitable environments, and can help to facilitate restoration by improving soil and hydrology.

Key practicesSpatial diversification to match the scale of a particular threat or stress at the field, farm or landscape scale emerged as a key strategy. Planting and maintaining stress-tolerant and diverse varieties across farms and landscapes is a traditional way to manage and spread risk,

Table 13. Contributions of diversification with crops at the landscape scale

Case study Shock or stress Reference(s)

In an agricultural landscape in northern Germany, the presence of old field-margin strips along rape fields and old fallow habitats was associated with increased parasitism and mortality of pollen beetles.

Pest damage Thies and Tscharntke, 1999

A review of landscape composition and natural pest control found that enhanced natural-enemy activity was associated with herbaceous habitats such as fallows and field margins in 80% of cases, with wooded habitats in 71% of cases and with landscape patchiness in 70% of cases.

Pest damage Bianchi, Booij and Tscharntke, 2006

A meta-analysis of 552 experiments found extensive evidence that herbivore suppression, enemy enhancement and crop-damage suppression were significantly stronger in diversified crops than in crops with no or few associated plant species.

Pest damage Letourneau et al., 2011

Permanent vegetation cover in non-crop habitat types such as forest, hedgerows, field margins, fallows and meadows provides refuge habitat for natural enemies.

Pest damage Tscharntke et al., 2007

In Vanuatu, farmers work numerous small fields in different locations in order to cope with hurricane and pest damage.

Hurricanes; pest damage

Blanco et al., 2013

Desert irrigation is maintained by planting in alluvial fans where rainfall and runoff are concentrated; tepary beans grown in this manner contain 12–23% more protein and provide more-consistent yields than those grown under conventional irrigation.

Water scarcity Nabhan et al., 1980

In Cuzco, Peru, different crop combinations and rotations are planted according to the agroclimatic belt to protect against crop loss from frost, drought or pests at different elevations.

Temperature extremes; pests

Brush, 2000; Gade, 1999

Waru-waru, raised fields surrounded by water-filled ditches, can minimize risk of flood, drought and frost, reduce soil loss and broaden cropping options.

Temperature extremes; flood and soil erosion

Altieri, 1999

Traditional landscape-management practices such as zais, bunds and contouring can improve microsite conditions and direct runoff towards planted areas, broaden cropping options and improve productivity and stability in marginal areas, but are often very labour-intensive.

Degradation; drought

Altieri, 1999; Roose, Kabore and Guenat, 1999; Dey and Sarkar, 2011

Spatial diversification of crops in small fields across a landscape maintains stability.

Environmental uncertainty

Blanco et al., 2013; Reidsma and Ewert 2008; Abson, Fraser and Benton, 2013

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Table 14. Contributions of landscape-scale interventions to resilience in forests, woodlots and silvopastoral systems

Case study Shock or stress Reference(s)

Diversification of silvopastoral systems with eucalyptus helped conserve rainfall with negligible soil loss; in community woodlots on degraded sites, fast-growing eucalypts perform well.

Degradation; water scarcity

Grewal et al., 1992; Jagger and Pender, 2003

Silvicultural approaches such as reduced-impact logging can help to minimize the collateral damage to forest structure and biodiversity and maintain the functionality of forests, including their ability to maintain ecosystem-service provisioning even during harvesting.

Damage during harvest

Guariguata et al., 2008

Beneficial interactions between trees, soil fertility and livestock help to stabilize production in farmed parkland systems, such as indigenous agroforestry systems in West Africa and the Sahel.

Degradation Pieri, 1989; Mortimore and Turner, 2005

Silvopastoral and dry-forest management helps improve and stabilize production in water-scarce areas.

Water scarcity Altieri, 1999

Integrated cattle–palm plantations in Southeast Asia improved complementarity of resource use, improving yields and restoring degraded landscapes; shade provided by the palms lowered temperatures and improved conditions for the cattle.

Heat stress Devendra, 2007; Johnson and Nair, 1985; Chen and Samsuddin, 1991; Das, 1991; Chen and Chee, 1993; Reynolds, 1995; Deocareza and Diesta, 1993; Liyanage de Silva et al., 1993

Shade lowers temperatures and reduces water loss from the soil in grazed babassu-palm agropastoral systems in northern Brazil, benefitting cattle.

High temperatures; water scarcity

Johnson and Nair, 1985

In northeastern Argentina, farmers have implemented silvopasture systems across 20 000 ha for timber, forage and cattle. Farmers have reported benefits including improved protection from frost and heat, reduced risk of forest fire and fewer pests and diseases.

Pests and diseases; temperature extremes; fires

Fassola et al., 2006 ; Frey, 2010

In Uruguay, over 500 000 ha of exotic forest plantations include a livestock component. The trees provide shade and shelter for the livestock, which in turn reduce the risk of forest fires.

Temperature stress; Forest fires

Cubbage et al., 2012

Agrosilvopastures in the southeastern United States of America can offset crop losses during extreme climatic events. In North Carolina, timber species planted in diversified agrosilvopastures provided a buffer in consecutive years of alternating floods and droughts that caused crop failure.

Floods and drought Glenn et al., 2011

In northern New Zealand, where winter rains contribute to erosion, Cryptomeria japonica is planted to provide shelterbelts to protect pasture and livestock.

Strong rain and wind; erosion

Cubbage et al., 2012

Integration of trees into range and pasturelands in Florida was shown to enhance nutrient retention in the system and reduce runoff of P, ammonium-N and nitrate-N to surface water.

Pollution Nair et al., 2007

Shelterbelts can reduce lamb mortality and abortions from winds, which raise the lower critical temperature for an animal, and increase the risk of hypothermia and mortality in new-born and recently shorn lambs and ewes.

Wind exposure Gregory, 1995

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for instance by matching varieties along agroclimatic gradients to optimize production in heterogeneous environments such as slope lands (Brush, 2000; Gade, 1999) or cropping along watershed features (Nabhan et al., 1980). Having fields at multiple sites protects farms against the effects of losses at one particular site (Reidsma and Ewert 2008; Abson, Fraser and Benton, 2013; Blanco et al., 2013).

Structural complexity of landscapes helps to manage pest and disease pressure. In agricultural landscapes with high pest pressure, utilization of habitat heterogeneity can enhance natural-enemy density and diversity to reduce crop damage relative to levels in simple landscapes where a high percentage of land is used for agriculture (Thies and Tscharntke, 1999; Bianchi, Booij and Tscharntke, 2006; Letourneau et al., 2011; Tscharntke et al., 2012). Beta diversity among vegetation patches determines natural-enemy distribution and maintains a diversity of generalist and specialist species in agricultural landscapes (Tscharntke et al., 2007).

Management and modification of landscape features can enhance resilience, particularly practices oriented towards conserving or managing the availability of resources such as water and soil and those oriented towards the modification of microclimates through the addition of biotic and abiotic features (e.g. bunds, hedgerows, ditching or terracing) (Altieri, 1999; Roose, Kabore and Guenat, 1999; Dey and Sarkar 2011).

An integrated approach combining assessments of diversity with analysis of farmers’ practices and strategies in macro- and micro-environments is important. Systems are affected by their environmental context and by farmers’ use and management of species and varieties. Multiscale studies suggest that agrobiodiversity alone is not an appropriate measure of the resilience of agroecosystems (Clergue et al., 2005; Blanco et al., 2013).

5.3.2. Forests, woodlots and silvopastoral systemsThe main mechanisms through which landscape-scale planting and conservation of trees in forests, woodlots and silvopastoral systems contributed to resilience included the following: enhancement of microclimate regulation, including moderating temperatures and humidity, improving nutrient cycling and stabilizing production of livestock and tree products at the landscape scale (Table 14). However, the case studies emphasized that proper planning and active management of silvopastoral systems are required in order to realize greater resilience to climate change (Cubbage et al., 2012).

Key practicesComplementarity in resource use and diversification into higher-value products increases profitability, nutrition and farm stability and productivity (Batugal and Oliver, 2005). Temperature stress can have significant impacts on livestock (see 5.1.3; 5.2.3). Shade provided by trees in pastures enhances the stability and productivity of livestock, while organic inputs provided by livestock can improve productivity in tree-crop production (Pieri, 1989; Mortimore and Turner, 2005; Altieri, 1999).

Regulation of the micro-environment, including the effects of trees on temperature, moisture and humidity and the effects of livestock on soil nutrient composition through the supply of organic manure, contributes to resilience (Devendra, 2007; Johnson and Nair, 1985; Chen and Samsuddin, 1991; Das, 1991; Chen and Chee, 1993; Reynolds, 1995; Deocareza and Diesta, 1993; Liyanage de Silva et al., 1993; Gregory, 1995).

Conservation of uncultivated woodland, including mangroves and other multipurpose agricultural wetlands, is important for the supply of non-timber forest products and other ecosystem services.

Diversification by planting new trees or enrichment of fallows increases the availability of non-timber forest products, fodder, food and other ecosystem services (Mortimore and Turner, 2005).

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Natural regeneration and circa situm conservation (protection of seedlings in landscape patches) by farmers facilitates continued evolution of locally adapted woody species (Dawson et al., 2013).

Preservation of woody biomass, both standing and fallen, in forested landscapes, helps to prevent soil erosion, enhances the diversity and abundance of wild and associated biodiversity through habitat provisioning, and in riparian corridors can improve water quality and reduce sedimentation (Altieri and Toledo, 2005).

5.3.3. Rangeland managementRangelands are highly dynamic and often non-equilibrium production systems that may transition in composition and state as a result of climate, disturbance regimes and grazing pressures. Both undergrazing and overgrazing can result in state changes. Mechanisms that confer resilience in pastoral rangelands are those that either contribute to maintaining the stability of a particular state through moderation of grazing pressures or contribute to adaptation to a change in state by expanding or altering transhumance ranges or by seasonal or periodic transition to alternative livelihoods such as crop production (Table 15).

Historically, inaccurate perceptions of rangeland ecosystems as stable equilibrium systems have been linked with the failure of development interventions in pastoralist systems (Ellis and Swift, 1988). Periodic changes in the composition of the natural vegetation are one of the defining features of many arid grasslands. Wetter rangelands can be more susceptible to overgrazing, while drier rangelands may be more resilient to grazing but are often affected by changes in climate (Reid, Fernández-Giménez and Galvin, 2014). The long-term absence of grazing can be a greater disturbance to rangeland than continuous grazing pressures (Oba et al., 2000).

The resilience of tropical grassland and rangeland systems is less studied than that of other production environments (Thornton et al., 2009). Better-understood impacts of climate change on rangeland resilience include the effects of increased temperature and reduced precipitation,

Table 15. Contributions of BFA to resilience in rangelands

Case study Shock or stress Reference(s)

Mobility of livestock helps to prevent overgrazing of pastures. Degradation Leisher et al., 2012

In the Gobi Desert, community-managed pasture showed significant improvements in plant production and cover of forage species.

Degradation Leisher et al., 2012

Maasai pastoralists rely on livestock diversification as one of the key adaptation strategies to survive highly variable climates and associated risk, utilizing species with different water and pasture requirements that will respond differently to diseases and climate extremes.

Disease; climate change;

Bobadoye, 2016

In pastoral societies, the key issues for sustainability and resilience are mobility, livestock diversity, livelihood diversification options, and preservation of pastoral traditions and indigenous knowledge.

Drought; climate change

Ayantunde et al., 2011

Multiyear droughts require new adaptation strategies that usually involve food substitution or expansion of the spatial scale of grazing.

Severe drought Ellis and Swift, 1988

In Kyrgyzstan, forests have traditionally provided cool air and fodder for livestock, but increases in temperature have made animals less productive. Shepherds have adapted by changing grazing locations seasonally.

Temperature stress

Kyrgyz shepherds and climate change

Sloping agricultural land technology (SALT) is an integrated system that includes strategies such as “screening and greening” (the planting of twin hedgerows of multipurpose woody legumes densely on slope-land contours), planting high-value crops and introducing small stock. An integrated-farming approach led to a 60-fold reduction in soil erosion in slope-land areas and tripled productivity and income.

Soil erosion Devadoss, Sharma Singh, 1985; Laquihon, 1995

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which are known to increase losses of domestic herbivores (Thornton et al., 2009). Driven in part by grazing, fire management and CO2 fertilization, woody plants are replacing grasses in rangelands worldwide with increasing frequency and with higher densities of invasive species (Reid et al., 2014). Difficulties in modelling the effects of increased CO2 levels on plant productivity and in determining changes in intra-annual precipitation patterns make long-term predictions of sustainability in semi-arid grazing systems difficult and unreliable (Tietjen and Jeltsch, 2007).

Key practicesTraditional knowledge contributes to the adaptable management of inherently variable rangelands and to appropriate use of BFA to maintain resilience (Bobadoye, 2016).

Management that considers the non-equilibrium nature of rangelands and other dynamic systems (e.g. slopelands) and variations in the state, composition and response of different pastoral agroecosystems is most effective for enhancing resilience (Reid, Fernández-Giménez and Galvin, 2014; Laquihon, 1995).

There is frequently a large social and political component to the resilience of pastoral systems. Often such systems involve migration across large transhumance zones that may cross political boundaries. Agropastoral systems frequently involve diversification into alternative livelihoods to manage risks and cope with losses (Leisher et al., 2012; Ayantunde et al., 2011).

Connectivity across landscapes, whether topographic, climatic or political, is important in enabling pastoralists to adapt their grazing and transhumance patterns (Ayantunde et al., 2011).

5.3.4. Marine fisheries and wetlandsMechanisms contributing to resilience in fisheries and wetlands focused heavily on maintaining stability and promoting recovery. Given the inherent complexity and strong ecological regulation underlying productivity in marine and wetland production systems, strategies were strongly centred around the maintenance of existing ecosystem function through conservation, and spatial diversification of the sites of exploitation, harvesting, breeding and reproduction to disperse risk across multiple sites (Table 16). As the lifecycles of many fisheries species involve multiple locations, conservation and protection across a wide range of aquatic ecosystems, including mangroves, seagrass beds and coral reefs, are critical to resilience strategies (Aburto-Oropeza et al., 2008).

Key practicesDiversification of fishing practices, including species targeted, locations and gear used, and diversification into alternative livelihoods, help prevent unsustainable fishing and buffer the livelihoods of fisherfolk against uncertainties and fluctuations in fishing stock (Vestergaard, 1996; Freire and Garcia-Allut, 2000).

Strong governance and social institutions frequently contribute to higher adaptive capacity in local fishing communities and lower sensitivity to change by maintaining livelihood options (Freire and Garcia-Allut, 2000; Vestergaard, 1996).

Conservation and restoration of coastal habitat, particularly mangrove forests, support production and minimize losses from shock (Aksornkoae and Tokrisna, 2004; Alongi, 2008).

5.4. Associated biodiversityBFA includes associated biodiversity that provides ecosystem services such as nutrient cycling and pollination to production systems. An increasing number of studies have explored the links between BFA and ecosystem function and services to understand the consequences of diversity loss for marine and terrestrial production systems.

The quality and quantity of ecosystem services are influenced by the composition, abundance and distribution of plant and animal communities at different spatial scales (Bianchi et al., 2006; Tscharntke et al., 2007; Hajjar, Jarvis and Gemmill, 2008; Quijas et al., 2012).

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In production systems, the presence of associated biodiversity can be encouraged through various management strategies and by the maintenance of relevant farm and landscape features (e.g. living fences and hedgerows). Examples of such approaches include erosion control, agroforestry, intercropping and pest-management methods such as IPM or push–pull strategies (Kahn et al., 1997; Pretty, 1999; Berg, 2004; Bohan et al., 2007; Chabi-Olaye et al., 2007; Dasgupta, Meisner and Wheeler, 2004; Ratnadass et al., 2012; Alam et al., 2012). The resilience of production systems depends, in part at least, on the resilience of species communities that provide ecosystem services (e.g. communities of soil biota and pollinators).

5.4.1. Soil-associated biodiversitySoil biodiversity (bacteria, fungi, protozoa and invertebrates) supports the delivery of ecosystem services such as water and nutrient cycling that maintain productivity and resilience in agroecosystems. New tools for biochemical and DNA analysis are improving our understanding of soil biodiversity. There is increasing evidence of the importance of soil biodiversity for the stability of production systems and their resilience to stress and disturbance (Brussaard, de Ruiter and Brown, 2007; Nielsen, Wall and Six, 2015; Sidibé et al., 2018). However, soil biodiversity is negatively affected by environmental changes and unsustainable management practices, and this can reduce its capacity to sustain ecosystem services essential for the resilience of above-ground systems (Wagg et al., 2014; Lal, 2015).

Table 16. Contributions of marine diversity to resilience

Case study Shock or stress Reference(s)

Small Danish fishery operations maintain flexibility through diversification of target species, gear types and fishing areas, and diversification into other forms of seasonal employment to supplement income.

Overharvesting Vestergaard, 1996

In northeastern Spain, artisanal Galician fisheries diversify their fishing practices, locations and gear and supplement income with wage labour to maintain flexibility.

Overharvesting Freire and Garcia-Allut, 2000

In West Java, individuals diversify their income from small pelagic fisheries with rice farming and tree crops to respond to dynamic seasonal and interannual variations in the availability of fish species.

Overharvesting Musa, Allison and Ellis, n.d.

Community-based restoration projects in the inner Niger Delta maintain nursery grounds for fisheries and provide pastures for cattle, improving resilience for local communities.

Habitat degradation

Wetlands International

Managing and protecting mangroves stabilizes and increases fisheries yields and household incomes.

Habitat degradation

Aburto-Oropeza et al., 2008

High levels of biodiversity at different trophic levels encouraged the recovery of coral-reef fisheries following bleaching events.

Habitat degradation

Cinner et al., 2013

Mangrove habitats retain soil moisture and help to moderate variation in local climates.

Mangroves perform a range of ecosystem services in multipurpose agricultural wetlands including nutrient cycling, habitat provisioning and increasing microbial decomposition.

Habitat degradation; temperature extremes

Vo et al., 2012; Pullin and White, 2011; Alongi, 2008

Mangroves in certain circumstances offer coastal systems limited protection from tsunamis, sea-level rise, hurricanes and coastal erosion. They can reduce wave flow pressure when forests are at least 100 m wide.

Storms Mangrove protection zones; Alongi, 2008; Aksornkoae and Tokrisna, 2004

In a study of 21 coral reefs following 90% loss of live coral cover, recovery was favoured when reefs were structurally diverse and in deeper water, had high density of herbivorous fish and juvenile corals and had low nutrient loads.

Coral bleaching Graham et al., 2015

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Through complex food webs (Brussaard, de Ruiter and Brown, 2007) soil biodiversity governs processes, such as decomposition of organic matter and cycling of mineral nutrients and carbon, that influence soil formation, structure and moisture. Under some circumstances, functional dissimilarity among species affects the efficiency of these soil-ecosystem processes more than species richness per se (Heemsbergen et al., 2004). Below- and above-ground biodiversity is closely interconnected (Eisenhauer et al., 2013). The stability of below- and above-ground processes is determined by diversity across trophic levels at both system (ecosystem or ecological community) and component (population, functional group or phylogenetic clade) levels (Proulx et al., 2010).

Studies of microbial communities can improve our understanding of the impact of environmental disturbances on soil systems and of processes of recovery (Hartmann et al., 2014). A number of studies of microbial diversity have made recommendations about practices that promote resilience in forests (Hartmann et al., 2014), shrublands (Kuske et al., 2012) or grasslands (de Vries et al., 2012) or about soil amendments that can increase resilience to heat stress, for example through improved water-use efficiency (Ouédraogo, Mando and Brussaard, 2006; Hueso, Hernández and Garciá, 2011; Hueso, García and Hernánez, 2012; Kumar et al., 2013).

The stability and resilience of soil microbial communities have been shown to result from a combination of biotic and abiotic soil characteristics; for example they can be determined by physico–chemical structure and its effect on microbial-community composition and physiology (Griffiths and Philippot, 2013). Studies by Rivest et al. (2013, 2015) suggest that agroforestry systems may have a positive effect on soil biochemical properties and microbial resilience, which in turn have a positive effect on crop productivity and tolerance to water stress, both droughts and floods. Other studies have shown that organic amendments increase soil organic matter content and hence increase the size and activity of the soil microbial biomass and help the soil to retain moisture (Hueso, García and Hernánez, 2012) and recover from water stress (Hueso, Hernández and Garciá, 2011).

Rhizosphere processes are essential for soil resilience against anthropogenic and natural perturbations (Lal, 2015). Symbiosis with mycorrhizal fungi improves plants’ ability to tolerate water stress and may stabilize or increase yields in association with efficient exploitation of soil nutrients (Furze et al., 2017). Root-mycorrhizae symbiosis in plants is resistant to moderate amounts of soil moisture stress, and benefits plants by increasing the transfer of mineral nutrients to roots during drought stress (Dwivedi et al., 2013). Arbuscular mycorrhizal fungi form mutualisms with many crop species, and these relationships are key to mitigating the effects of abiotic stress in many agricultural systems (Furze et al., 2017). Interactions between legumes, nitrogen-fixing bacteria (e.g. rhizobia) and mycorrhizal fungi are generally considered to benefit nitrogen uptake by legumes, but can also improve performance in variable and stress-prone environments (Oruru and Njeru, 2016).

Climate and habitat changes will affect earthworms, ants, termites and other animals that mediate soil processes such as nutrient cycling and thereby sustain agroecosystem productivity (Bates et al., 2013; Nielsen, Wall and Six, 2015; Del Toro, Ribbons and Ellison, 2015). The impact of environmental change on soil fauna may vary across taxonomic groups (Schon, Mackay and Minor, 2012). By helping maintain soil structure and supporting nutrient cycling, soil fauna can contribute to ecosystem stability under stress. For instance, landscapes with fields of termite mounds may be more drought-resilient, as termite nests alter soil properties in a way that enhances plant growth in dry conditions (Bonachela et al., 2015). Table 17 presents case studies on the ways in which different types of soil biota contribute to resilience through positive effects on water availability and disease control.

Key practicesRestoring and increasing the diversity of above-ground vegetation through crop rotation, intercropping, agroforestry, diversified crop cultivars and preservation of field margins, hedges and biodiversity refuges.

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Use of beneficial soil organisms through addition of organic manure, nitrogen-fixing leguminous species, microbial inoculants, mycorrhizas (spores, hyphae and root fragments), earthworms, etc.

Maintaining and improving soil structure through the presence of macro-invertebrates can facilitate microbial processes and improve the biochemical properties of soils.

5.4.2. Pollinator biodiversityWild and managed pollinators, which provide a wide range of benefits and contribute to the maintenance of wider biodiversity and ecosystem stability, continue to face numerous threats, including habitat loss, climate change and pesticides (IPBES, 2016). According to IPBES (2016), adaptive responses to climate change include increasing crop diversity and regional farm diversity, and targeted habitat conservation, management or restoration. As further discussed below, the available evidence suggests that abundance and diversity of pollinators improve pollination efficiency and increase the stability of pollination services in the context of temperature and rainfall variability and changing seasonal patterns through complementarity and functional synergy.

An increasing number of empirical studies show that wild pollinator species help to stabilize the flow of pollination services (Greenleaf and Kremen, 2006a,b; Winfree and Kremen, 2009; Rader et al., 2016; Table 18) and provide insurance mechanisms in the context of climate variability and change (Christmann and Aw-Hassan, 2012), particularly through response diversity (Fründ et al., 2013). Response diversity among pollinators can help to maintain plant–pollinator phenological synchrony, in the face of changes in temperature and shifting seasonal patterns associated with climate change (Garibaldi et al., 2013). The maintenance of functional and response diversity in pollinators requires habitat protection and restoration and low use of agrochemicals (Brown and Paxton, 2009; Batáry et al., 2013; Jakobsson and Ågren, 2014; Andersson et al., 2014; Fontaine et al., 2006; Hoehn et al., 2008; Blüthgen and Klein, 2011). While uncultivated areas at the field level, for example field margins, act as important habitats for pollinators (Benjamin, Reilly and Winfree, 2014), the abundance of pollinators in such fragments has been shown to decline with distance to larger

Table 17. Contributions of soil diversity to resilience

Case study Stress or shock Reference(s)

Agroforestry may increase soil-microbial resilience to wetting–drying perturbations and drought.

Wetting–drying perturbations and drought

Rivest et al., 2013, 2015.

Organic amendments increased soil organic matter content, hence improving the size and activity of the soil microbial biomass and helping the soil to retain moisture and recover from water stress.

Water stress Hueso, Hernández and Garciá, 2011; Hueso, García and Hernánez, 2012

Fungistasis is an important means of controlling soil-borne plant pathogens. Soil fungistasis is correlated with soil bacterial community composition and diversity.

Control soil-borne plant pathogens

Minna et al., 2008; Garbeva et al., 2011 ; Koller et al., 2013

Soil microbial diversity improves nutrient cycling and water retention, which contribute to tolerance of, and recovery from, water stresses and drought.

Drought Jurburg et al., 2018; Minna et al., 2008; Brussaard, de Ruiter and Brown, 2007; Ouédraogo, Mando and Brussaard, 2006

Intercropping with legumes increased the resilience of soil microbial and nematode communities.

Water stress Sun et al., 2018

The presence of mycorrhizal fungi stabilizes production during drought and nutrient insufficiencies.

Water stress Furze et al., 2017; Davies, Calderón and Huaman, 2005; Fonte et al., 2012

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natural and semi-natural habitats (e.g. grasslands, forests, woodlands or fallows) in landscape mosaics (Korpela et al., 2013; Andersson et al., 2014; Jakobsson and Ågren, 2014).

Pollinator diversity is also important in grassland production systems, including meadows and pastures. Grassland plants dependent on insect pollination are affected by increasing land-use intensity (Clough et al., 2014) and by climate change, and both of these can alter the species composition and adaptive potential of such plants and consequently of pollinators (Hoiss et al., 2012). In northern Europe, management intensification and increased nutrient (nitrogen) input have altered grassland-plant communities, their species diversity and their functional-trait composition over the last several decades. This has resulted in a decrease in abundance of insect-pollinated flowering herbs and of insect pollinators (Wesche et al., 2012). Studies show that the density and diversity of pollinators depend on the type of grassland management: organic management of crop fields, meadows or pastures generally supports higher species richness and cover of insect-pollinated plants, which has a positive effect on the density and diversity of bees and other pollinators (Batáry et al., 2013).

Key practicesFarming practices that reduce chemical inputs; increasing farm diversity through intercropping; inclusion of flowering crops in crop rotations; agroforestry.

Maintaining natural or semi-natural habitats in, or adjacent to, production systems to provide nesting and alternative foraging resources

Diversification and weed management, by means of enhancing floristic diversity in grasslands and other production systems.

5.4.3. Associated biodiversity for fisheriesAssociated biodiversity contributes to the stability and resilience of ecosystems that support fisheries, such as coral reefs, mangroves and other wetlands (Hughes, 2004; Hughes et al., 2005; Brotherton and Joyce, 2014; Table 19). For instance, in coral-reef fisheries, high levels of biodiversity at different trophic levels encouraged the recovery of coral fisheries from bleaching (Cinner et al., 2013; Table 20). The ways in which the diversity of different trophic groups stabilizes a coral reef system are complex and interrelated, and system resilience can be compromised by a balance shift at any scale (Table 19). In seagrass systems, high species richness was linked to greater capacity to ensure the sustainability of ecosystem functions under disturbance or change through complementarity in resource exploitation (Duarte, 2000), and high genetic diversity improved resistance to disturbance (Hughes, 2004).

Table 18. Contributions of pollinator diversity to resilience

Case study Contribution to resilience

Reference(s)

Wild-pollinator abundance and diversity improve pollination efficiency and increase stability and productivity through complementarity and functional synergy.

Stability of pollination services

Brittain et al., 2013; Greenleaf and Kremen, 2006a,b; Aouar-sadli, Louadi and Doumandji, 2008; Julier and Roulston, 2009; Kasina et al., 2009

Foraging places and nesting sites for solitary and social bees, and crops with floral attractiveness and rewards for insects, can enhance pollinator conservation, as well as yield stability.

Palmer et al., 2009

Landscape complexity and maintaining natural or semi-natural habitats in, or adjacent to, production systems to provide nesting and alternative foraging resources improve pollinator efficiency and diversity.

Carré et al., 2009; Heard et al., 2007; Bartomeus et al., 2014; Morandin et al., 2007; Ricketts et al., 2008; Klein et al., 2003; Klein, Steffan-Dewenter and Tscharntke, 2004

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More-recent studies have shown the importance of taxonomic, phylogenetic and functional diversity in coral reefs for sustained ecosystem functioning and the associated supply of ecosystem services, including seafood provisioning, as illustrated in Table 20 (D’agata et al., 2014; Micheli et al., 2014). These studies contributed to the accumulating empirical evidence that overfishing can impair ecosystem resilience by reducing diversity (Mumby et al., 2007). For instance, reduction in parrotfish populations as a consequence of fishing, negatively affects their ability to control macroalgae and in turn the resilience of coral reefs (Lokrantz, Nyström and Thyresson, 2008).

A number of studies showed that the genetic diversity of marine communities affects the stability and resilience of marine ecosystems (Table 19). For instance, studies of the genetic diversity of the seagrass species Zostera noltii (Massa et al., 2013) and Zostera marina (eelgrass) (Hughes and Stachowicz, 2009) indicated that genetic richness has a positive effect on recovery from stresses and on performance under stress. While these and other studies (e.g. Reynolds, McGlathery and Waycott, 2012) indicated the importance of taking

Table 19. Contributions of associated biodiversity in marine ecosystems to resilience

Case study hock or stress Reference(s)

Hybridization contributes to evolution and adaptation to environmental change in coral reefs.

Environmental change

Willis et al., 2006

Genetically diverse communities recover from shocks and disturbances more quickly than uniform ones.

Shocks and disturbances

Massa et al., 2013; Pullin and White, 2011; Reusch et al., 2005; Reynolds, McGlathery and Waycott, 2012; Parkinson and Baums, 2014

Protection of multispecies assemblages helps to maintain marine ecosystem functions and services.

Environmental change

D’agata et al., 2014, Micheli et al., 2014 ; Mumby et al., 2007 ; Lokrantz, Nyström and Thyresson, 2008 ; Cinner et al., 2013

Table 20. Interactions between species, traits and resilience in coral-reef fisheries

Organism/group Trait or response Impact upon ecosystem

Calcifying organisms

Diversity/proportion Calcifying organisms help reefs with cementation, recruitment and settlement, and increase recovery following disturbance.

Coral Sensitivity to bleaching

Some species of branching or plating corals are more severely impacted by bleaching than others; higher abundance of these susceptible species confers higher sensitivity to the ecosystem.

Area cover Coral cover is linked to increased resilience and recovery.

Size class Evenness across size classes increases recovery.

Species richness Coral species richness can promote recovery.

Fish Sensitivity to disturbance

Some fish are more heavily impacted by disturbance than others; higher abundance of these species confers greater sensitivity.

Biomass Ecological metabolism and potential growth increase with biomass.

Richness Functional redundancy promotes recovery.

Size distribution Large individuals, in particular, can increase fecundity and promote fish-community recovery.

Macroalgae Surface area Macroalgae limits coral recovery post disturbance by increasing competition for substrates, allelopathic activities and smothering coral by trapping substrates.

Herbivores Abundance Increased herbivory by fish and urchins reduces macroalgae and increases coral recruitment; it can shift reefs from coral decline to coral recovery.

Source: Based on Cinner et al. (2013).

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intraspecific as well as interspecific diversity into account in management and restoration plans, further research is needed on the factors affecting resilience to biotic and abiotic stresses (Hughes and Stachowicz, 2011). Recent studies have shown that genetic diversity, like species diversity, can influence resilience through a complex mix of dominance and complementarity mechanisms (Hughes and Stachowicz, 2011).

Key practicesMaintaining high levels of diversity, including genetic, species, functional and response diversity.

Maintaining adequate population sizes, including representation of all size and age groups, by reducing harmful practices such as overfishing and minimizing collateral damage to reefs and other crucial breeding habitats.

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6. Livelihoods, food security and nutrition

Improving the resilience of production systems is linked to a wider set of development goals that include improving livelihoods, food security and nutrition. In the studies reviewed in this paper, the contribution of BFA to resilience is frequently linked to specific livelihood, food-security and nutrition objectives or outcomes. The interrelationships between BFA, resilience and other development goals are complex. BFA may contribute to some aspect of resilience and, as a result, improve livelihoods and food security and nutrition (Table 21). Alternatively, BFA may contribute directly to these goals and thus improve resilience. For more on interrelations between agroecosystem resilience and other production-system goals, see Cabell and Oelofse (2012).

The complex nature of the interrelationships may be illustrated with reference to agroforestry and non-wood forest species (Sections 5.2.2, 5.3.1). These species improve resilience, especially in the context of climate change (Mijatović et al., 2013), and contribute to improving nutrition and the sustainability of production systems (Vinceti et al., 2013; Nguyen et al., 2013). However, agroforestry products such as non-timber forest products (NTFPs) can be subject to overexploitation, the actions of intermediaries and fluxes in availability and quantity. A strategy focused on improving production or diversity of NTFPs may not help to reduce poverty (Belcher, Ruíz-Pérez and Achdiawan, 2005), and may even serve as a poverty trap (Dove, 1993; Brondizio, 2008). Similarly, in the case of livestock and crops, while traditional breeds may improve resilience and the capacity to cope with temperature or water stress resulting from climate change, they may also reduce the overall productivity of a system and lower farmer incomes (see Sections 5.1.1, 5.1.3). Nonetheless, BFA is an important element of securing livelihood, food-security, nutrition and sustainability goals. In this section, the focus is on the case studies demonstrating when and how improved resilience resulting from the use of BFA has contributed to outcomes such as sustainable livelihoods and food security and nutrition.

6.1. Rural livelihoodsLivelihoods comprise “the assets (natural, physical, human, financial, and social capital), the activities, and the access to these (mediated by institutions and social relations) that together determine the living gained by the individual or household” (Ellis, 2000). Sustainable livelihoods are those that are able to withstand stresses and shock, maintaining and enhancing present and future capabilities, without undermining the natural resource base (Scoones, 1998). BFA is recognized as making an important contribution to sustainable rural livelihoods, including by generating different forms of capital and influencing activities and enterprises undertaken by the household (e.g. Giuliani, 2007).

Table 21. Main benefits of resilience-enhancing practices to livelihoods and food security

Sustainable livelihoods

Improving option values from diversified whole-farm output

Improving stability of production

Providing self-insurance against shocks

Reducing inputs such as nutrients, water and energy

Increasing household income

Providing opportunities for on-farm employment and livelihood diversification

Food security and nutrition

Stabilizing and increasing yields and production

Local crops, varieties and animal breeds with higher nutrition value

Diversifying diets

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The case studies presented in Section 5 showed that BFA can improve resilience-related properties not only of natural capital but also of the other livelihood assets. Diversification was a common general strategy for improving nutrition and income, in which animal production played an especially important part. Animal ownership was shown often to be a key livelihood asset. Combining resilience and livelihood-enhancing strategies was a frequent element of the case studies from mixed farming systems (Section 5.2; Tables 8–13). Diversification was also shown to generate opportunities for production of higher-value products or those with complementary seasonality to others. The creation of new farm enterprises, such as dairying, vegetable farming, aquaculture and cattle fattening, benefited rural livelihoods through the creation of local jobs (Tables 11−13). The diversification of farms with livestock reduced labour requirements where animals could provide traction. Aquaculture benefited households by providing large gains in income where there were nearby markets (Tables 11, 13). Diversification into higher-value crops and products such as vegetables, fish or seeds had pronounced benefits for women, who were able to draw upon additional economic opportunities within existing production systems (Tables 10–13).

BFA-based strategies at the field and farm level can have important benefits for women, who often employ different coping strategies from men. Female-headed households may often be more vulnerable to shocks than male-headed ones (Niehof, 2004). In Zimbabwe, female-headed households experienced significantly less recovery than male-headed households following drought (Bird and Shepherd, 2003). In Mozambique, women were found to dominate activities such as local trade, casual employment and vegetable cultivation, usually locally and at a small scale, but to be less involved in livestock sales, charcoal production and produce sales to urban markets (Eriksen and Silva, 2009). Ayantunde et al. (2011) also reported on gender-specific diversification strategies, whereby men were more likely to enter into wage labour and women more likely to diversify into petty trade of products such as milk, vegetables, handicrafts and beer. BFA-based approaches to improving resilience will need to take account of gender-based differences and the different roles of different BFA components for men and women.

6.2. Food security and nutritionFood security is said to exist when all people at all times, have physical, social and economic access to sufficient, safe and nutritious food in order to meet their dietary needs and food preferences for an active and healthy life (FAO, 2011). Over the last few years, fluctuations in food prices and availability in a number of countries have shown how vulnerable the global food system remains and that improving its resilience in terms of the four pillars of food security (availability, access, utilization and stability) (FAO/IFAD/UNICEF/WFP/WHO, 2018) remains a global development objective.

BFA at different scales has been demonstrated to contribute to each of the four pillars and to improving the resilience of food systems (Mouillé, Charrondière and Burlingame, 2010; Frison, Cherfas and Hodgkin, 2011; DeClerck, 2013), and many of the case studies directly noted the contribution of BFA to food security and nutrition. Most of these studies associated diversity with improved dietary diversity, such as the contribution of animal products in mixed-farming systems and fish in aquaculture–crop systems to the supply of protein, vitamins and minerals. Examples included those that showed that low species richness on farms and low nutritional diversity corresponded with low dietary diversity, high food insecurity and a high number of months of inadequate food provision (Remans et al., 2011) and those that demonstrated the contributions of dietary diversity, including fruits and vegetables, animal-source foods and legumes, to health (Johns and Staphit, 2004; Arimond and Ruel, 2004; Frison et al., 2006). Empirical work on links between production diversity and consumption diversity is, however, limited, and other factors complicate the relationship. Market transactions have been shown to have a higher effect on dietary diversity than production diversity, and increasing on-farm

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diversity or biodiversity in the surrounding landscape may not always lead to higher dietary diversity (e.g. Sibhatu, Krishna and Qaim, 2015).

The various categories of BFA have each been shown to contribute to improving food security and nutrition and to the resilience of food systems through their contributions to availability, accessibility, utilization or stability. Minor grains, fruits and legumes all make important contributions to improving food security and its resilience (Smith, 1982; Vuong 2000; Luximon-Ramma, Bahorun and Crozier,2003; Sundriyal and Sundriyal, 2004; Pudasaini et al., 2013). Leafy cultivated or wild vegetables are also an important source of micronutrients (Heywood, 2011). Crop genetic diversity makes an important contribution to food security and nutrition, improving the availability and utilization of nutritious foods and the stability of production (Burlingame, Mouillé and Charrondière, 2009; Lutaladio, Burlingame and Crews, 2010; Heywood, 2011; Dwivedi et al., 2012; Khoury et al., 2014).

As the quickest-growing sector of food production, aquaculture provides a promising way of improving food security. Approximately 90 percent of total aquaculture production is in food-deficit developing countries, with a high proportion accounted for by small-scale production (Zeller, Booth and Pauly, 2007). In the Democratic Republic of the Congo, where households are increasingly dependent on livelihood diversification into extractive subsistence activities in the absence of markets, women use a traditional collective fishing method involving basket-traps during the dry season. Although the quantity of fish caught by women is usually smaller than that caught by men, 60 percent is kept for household consumption compared with 27 percent of that caught by men, making women’s fishing an important contributor to household food security (Béné et al., 2009) and to complementary livelihood strategies important for resilience.

Livestock make a substantial contribution to livelihoods in many societies around the world and contribute importantly to food security and nutrition. Table 6 notes the importance of locally adapted breeds and their performance under stressful conditions and lower food intake. The ways in which within-species diversity in goats can be used to secure continuing lactation and to improve parentage were also noted (Lanari, Pérez Centeno and Domingo, 2007). The integrated management of pasture and livestock to maximize food security and nutrition outcomes in mixed-farming and pastoral systems under stress was also reported (Tables 12, 14, 16).

At local level, wild-harvested foods continue to play an important role in food security and nutrition and in the resilience of local communities, especially in providing food in times of shortage and drought or during the hungry season between harvests (Fleuret, 1979; Shackleton and Shackleton, 2004). A survey summarizing information from 36 studies in 22 countries reported that around 90 to 100 wild species were used on average and that in some instances estimates of the numbers of wild food species utilized can reach 300 to 800 (Bharucha and Pretty, 2010). Foraging for wild foods has been described as an important factor in reducing vulnerability and alleviating food insecurity in Lesotho (Adger, 1999), coastal Viet Nam (Fleuret, 1979), Ghana (Codjoe and Owuso, 2011) and the United Republic of Tanzania (Enfors and Gordon, 2008). Both animal (terrestrial and aquatic) and plant species can be important sources of wild-harvested foods.

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7. Conclusions

The aim of this thematic study was to review literature on the contribution of BFA to the resilience of production systems to environmental change, variability and uncertainty. Section 5 summarized the evidence that links BFA to the resilience of different components of production system at genetic, species and ecosystem levels. Section 6 discussed how resilience-strengthening BFA practices can improve livelihoods, food security and nutrition. This concluding section summarizes the main ways in which BFA enhances the resilience of production systems, identifies knowledge gaps and provides some recommendations on how BFA can be used to improve resilience in production systems.

7.1. Main findingsThe results from the review support the view that resilience against a broad range of stresses requires the integration of multiple BFA-based strategies at different scales. The analysis shows that BFA contributes to the resilience of production systems by: (i) providing resistance to, or tolerance of, shocks and stresses; (ii) supporting adaptation; (iii) maintaining stability; and (iv) supporting recovery from disturbances. These contributions are interrelated and involve interactions between genetic, species and ecosystem diversity at different spatial scales.

7.1.1. Resistance to or tolerance of shocks and stressesGenetic diversity in crops, animals and aquatic species (and in some cases associated biodiversity) enhances resilience by providing resistance to, or tolerance of, abiotic or biotic stresses and shocks, and by providing diversity in responses to changes in the nature and level of stresses. Resilience may be enhanced by traits that increase tolerance of changes in abiotic conditions (e.g. temperature or salinity), resistance to, or tolerance of, pests and diseases, or capacity to recover from extreme drought, frost or other shocks. For aquatic species, this could mean tolerance of lower water quality and toxic blooms. Phenotypic plasticity emerged as an important trait for resilience. In crops and trees in particular, and probably in other types of organisms, phenotypic plasticity can help adjust the timing of key phenological events, which will be disturbed by changing seasonal patterns. Identifying genetic diversity underlying adaptive traits will be critical to increasing the contributions of breeding and conservation programmes to resilience. This has been facilitated across all sectors by developments in genetic and genomic profiling.

7.1.2. Adaptation and continued evolutionThe maintenance of genetic diversity supports continued evolution and helps to ensure that varieties, breeds, populations and species are able to adapt to changed conditions. These processes involve the generation of new genes and combinations of genes in response to stresses and variability. The extent and nature of evolution are influenced by natural selection and by human activities and management, including, for example, by the extent to which we allow processes such as gene flow and recombination to generate new variation. The review identified a number of cases, such as the changing characteristics of traditional varieties of sorghum and pearl millet in Mali and Niger, that provided evidence of the importance of continuing evolution as part of adaptation to climate change (Vigouroux et al., 2011). Adaptation was also found to be important at species and landscape scales, for example in the increasing use of agroforestry species in adaptation to climate change, the changing mix of crops and animals in some production environments, and the movements of aquatic species to new environments. Corridors and connectivity across landscapes are critical in maintaining short-term adaptation, including movement of herds to track available resources and favourable climates, and long-term adaption through continued evolution. Assisted migration, provenancing and use of

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pre-adapted germplasm in restoration efforts are among ways of maintaining adaptive capacity over longer time scales. Breeding programmes across sectors are increasingly focusing on identifying and incorporating traits relevant to adaptation to climate change.

7.1.3. Stability of production systems and ecosystem services under multiple stressesGenetic and species diversity including associated diversity, and ecosystem diversity at the landscape scale contribute to the stability of production systems by buffering against stresses (e.g. extreme weather events, droughts and temperature fluctuations). For example, agroforestry was shown to reduce exposure to climate risk and variability (e.g. by buffering the impact of hurricanes on crop loss) and to provide services such as soil-erosion control and nutrient cycling through above-ground and below-ground interactions. Other traditional BFA-based practices demonstrated to help manage risk and stabilize production included:

• pest and disease regulation utilizing crop mixtures (species mixtures as well as variety mixtures);

• various types of integrated systems including trees, annual crops, animals and aquatic species at both farm and landscape/seascape scales; and

• complementary use of resources at the landscape/seascape level, for example the integration of diverse production systems (animal, crop, aquatic) across the landscape/seascape gradient.

Associated biodiversity contributes to stability through continuing provision of essential ecosystem services, whose flow is determined by functional biodiversity, including functional complementarity and redundancy. For example, functional synergies between honey bees and wild pollinators contribute to improved pollination services and help to maintain plant–pollinator synchrony disrupted by changes in seasonal patterns. Habitat protection through the maintenance of complex landscapes/seascape seems critical for maintaining functional diversity. In terrestrial ecosystems, appropriate combinations of below-ground and above-ground diversity can help buffer the effects of water stress on grassland and cropland productivity.

7.1.4. Recovery following disturbanceDiversity at all levels, including associated diversity, influences the capacity of production systems to absorb minor shocks and stresses as well as to recover from severe disturbances (e.g. hurricanes). The rate of recovery is determined by biophysical (e.g. biodiversity) as well as social and cultural factors. While recovery may involve a “return” to the former taxonomic composition, structure and ecological functions of the production system, it may also provide opportunities for novelty and innovation resulting in adaptation or a transformation of the system’s social or biological components. An example would be the development of new community-based institutions to guide large-scale restoration and facilitate the adoption of alternative, more sustainable, livelihood approaches.

7.2. Research and knowledge gapsThe review has identified a number of important knowledge gaps, the most important of which are listed in this section.

7.2.1. Responses to and recovery from disturbancesAmong the various ways in which BFA contributes to resilience, its contribution to capacity to recover is the most under-researched. Very few studies explore the contribution of BFA to recovery from stresses and how it can be better harnessed in the restoration of production environments, particularly in intensively managed systems. More research is needed on responses to, and adaptation strategies for, increased climate variability, including greater fluctuations in temperature and rainfall and changing seasonal patterns. Studies looking at recovery in extensively managed ecosystems such as coral reefs and grasslands can provide

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insights into how to study recovery in intensively managed systems. A small number of studies have focused on the response of natural ecosystems to management practices and disturbances (e.g. hurricanes, coral bleaching and drought). More research specifically focused on the role of BFA is needed to guide management and restoration efforts.

7.2.2. Integrating across scales and components over timeMany of the studies reviewed focused on a single BFA component or aspect of a specific system rather than on the resilience of the entire system. Approaches that can integrate information and experiences across scales and components from a resilience perspective are needed. Furthermore, across a range of production systems the literature is dominated by studies that involve short-term periodic measures of performance, focusing on yield. However, building resilience is a dynamic process that involves adaptation and innovation. Long-term studies are needed that include analysis of responses and interactions between the different factors contributing to resilience.

7.2.3. Achieving transformation towards diversity-rich production systemsDespite the knowledge gaps mentioned above, the resilience-strengthening practices identified in this review are widely recognized (e.g. IPBES, 2016; FAO, 2016). In addition to further empirical evidence of the contribution of BFA to resilience, a key priority is to better understand how to promote these widely recognized practices and how to transition towards diversity-rich production systems. Development of strategies for promoting resilience-strengthening practices can benefit from better understanding of the dynamics of production systems using the social-ecological resilience lens. This will require resilience assessments that aim to identify locally appropriate management strategies that enhance resilience. This will involve research that takes account of the multiple components of BFA and social-ecological resilience (e.g. innovation, traditional knowledge and social capital). It will therefore need to be transdisciplinary and involve the direct participation of local communities and the many different sections of society that are involved.

7.3. RecommendationsMany production systems have lost BFA through the continuing trend towards monocropping, the replacement of soil biodiversity with external inputs, and the simplification of landscapes and seascapes resulting in the disappearance of natural and semi-natural components. Degradation and biodiversity loss in crop, animal, forest and aquatic production systems may severely compromise ability to maintain productivity under environmental change and climatic variability. This review suggests a number of ways in which BFA can contribute to enhancing resilience. These involve actions in three main areas:

• conservation and availability of genetic and species diversity to support adaptation and diversification, including the characterization and evaluation of traits linked with resilience;

• diversification of production systems to manage risks and mitigate the impact of environmental change and variability on production; and

• habitat restoration for landscape/seascape complexity to support the conservation and flow of ecosystems services and the capacity of production systems to absorb and recover from disturbance.

These three approaches are interrelated and mutually supportive of resilience. Specific actions in these three areas need to build on ecological understanding and the principles of sustainable management and resilience theory.

The actions should aim to support:• In situ conservation of diverse populations of tree species, aquatic species and crop

wild relatives, as well as of traditional breeds and varieties. Such populations provide

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essential options for adaptation and continued evolution. Equally important will be conserving diverse populations of associated species of pollinators, soil biota and other organisms in croplands, grasslands, wetlands, forests and marine ecosystems that support food production. These species also need to be able to adapt to change and uncertainty.

• Diversification on farms and in fields, incorporating both the conservation of local resources and improved access to new resources and knowledge. Successful diversification initiatives will require access to resources (e.g. germplasm, tools and technologies, and often capital or credit) together with training and transfer of knowledge on both the abiotic features of the landscape and the requirements and tolerances of the various biotic components within the production system.

• Improving response diversity in crops, trees, livestock and aquatic species to account for climatic variability and predicted future conditions. This can be achieved through maintenance of high genetic and species diversity as well as moving beyond breeding and improvement efforts targeting single traits or functions and towards multitrait selection.

• Increasing functional diversity through adoption of practices based on enhanced use of associated biodiversity. This will make an essential contribution both to resilience and to ecofunctional intensification. There are also opportunities to make greater use of genetic and species diversity in practices that are well tested and are part of sustainable agriculture or agroecology, for example expanding the use of diversity in IPM programmes, and to give increasing attention to the use of associated diversity in soil- and nutrient-management programmes.

• Harnessing complementarity and environmental heterogeneity. Complementarity in production and use through diversification at all scales supports resilience. At the landscape/seascape scale this includes utilizing appropriate spatial or temporal arrangements, as well as species and genetic complementarity, to improve the resilience of crop, animal, agroforest and aquatic production. It also includes utilizing the complementarity of above- and below-ground associated biodiversity in harnessing services such as nutrient cycling and pollination (e.g. endosymbiosis of roots and nitrogen-fixing organisms, larval life stages of some invertebrates).

• Recognizing that multifunctionality of landscapes/seascapes underpins many of the services they provide and their contributions to recovery and to habit provisioning and connectivity critical for wild flora and fauna, including invertebrates and micro-organisms. For example, wetlands can support a wide diversity of wild, farmed and feral aquatic species that perform a range of ecosystem services for agriculture, livestock keeping and inland fisheries, including flood regulation. Wetlands also harbour crop wild relatives with stress-related traits of importance for adaptation and long-term evolution.

• Mobility and migration (natural and assisted) and the movement of populations or particular types to new environments. Both natural and assisted migration and the introduction of new materials will play an increasingly important role in meeting the challenges of climate change. The latter will involve building on the gains made on access to genetic resources for food and agriculture through, for example, the Nagoya Protocol. The maintenance of connections among forest landscapes by reducing fragmentation, recovering lost habitats and expanding protected area networks can make an important contribution to the resilience of production systems and the provision of ecosystem services.

• Adoption of the participatory and transdisciplinary approaches that will be needed to develop and promote locally appropriate resilience-strengthening strategies. Community-based assessments that can be accomplished in reasonable time scales

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and produce tangible results will need to be combined with long-term studies of, for example, the evolution of local varieties, breeds and populations in marginal environments and the complex nature of genotype by environment interactions.

• Integration of local knowledge into resilience activities within an SES framework. Most BFA is managed by farmers, forest dwellers, pastoralists, fishers and rural communities, and strategies for using BFA to improve resilience will need to be locally appropriate. This will require integrating local knowledge derived from experiences of coping with harsh and fluctuating environmental conditions.

• Further research on resilience, including in the following areas: analyses of the ways in which BFA can optimally contribute to responses to, and recovery from, stresses and shocks (the development of guidelines on “BFA and pathways to resilience”); development of approaches that integrate effects at different scales and that involve diverse components of BFA; studies that assess the contribution of BFA to resilience of production systems over time periods that are long enough to capture medium- and long-term outcomes; and fuller analysis and description of the dynamic nature of production systems and how to promote resilience-strengthening practices.

• Greater institutional and policy support for wider adoption of diversity-rich practices that contribute to resilience. There is already an extensive body of knowledge that indicates the many different ways in which resilience in production systems can be strengthened. An institutional and policy framework is needed that can support the efforts of farmers, fishers, forest dwellers and pastoralists to strengthen resilience in their respective circumstances.

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Glossary

Adaptive capacity – the capacity of a system to adapt, shaped by the interaction of environmental, social, cultural, political and economic forces.

Component (of BFA) – in the context of this study, component refers separately to animal, aquatic, crop or forest biodiversity or to the insect, bacterial, fungal or other major elements of associated biodiversity.

Degradation – deterioration of a particular environment as a result of depletion of biotic or abiotic resources or pollution, through, for example, the presence of excess nitrogen, heavy metals or pesticide or herbicide residues.

Environmental change – we consider environmental change to include climatic change and variability, shocks and stressors, slow-onset events and environmental degradation.

Functional diversity – the value and range of the functional traits of the organisms in a given ecosystem.

Level – in the context of this study, level refers to the biological unit for analyzing contributions of BFA to resilience, and includes genetic diversity within a species (i.e. populations, ecotypes, breeds, landraces, etc.), species, mixed-species assemblages and diversified systems (i.e. agroforests, on-farm aquaculture, etc.)

Phenotypic plasticity – changes in an organism’s morphology or physiology as an adaptation to changes in its environment.

Resilience – in this study resilience is defined as the capacity of a system to absorb stresses and shocks and maintain function in the face of environmental changes and uncertainty (inclusive of stressors and variability) and evolve into a system capable of withstanding a wide range of future conditions.

Resistance – the ability of an organism to remain unaffected by exposure to a stress, often in reference to a genetic advantage against a particular biotic or abiotic stressor.

Response diversity – response diversity refers to species assemblages, species and varieties that perform similar ecosystem functions but have different capacities to respond to disturbance or fluctuations.

Shock – an extreme or sudden climate or weather event (e.g. a severe drought, flood, heat shock, fire or storm) or other major disturbance that disrupts the function or stability of a socio-ecological system.

Stability – reduction in variability, often as an outcome of self-regulating capacity. In agricultural systems, stability is usually described as low variability in yield over space or time.

Stress – perturbances that decrease the fitness of components in a socio-ecological system.

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Scale – in the context of this study, scale refers to the defined spatial unit used to analyse contributions of BFA to resilience: the field, farm, village, landscape and country are different scales.

Slow-onset events – manifestations of climate change that evolve gradually from incremental changes over years or from increased frequency or intensity of recurring events. They may include desertification, rising temperatures, salinization, coastal sea-level rise, ocean acidification, and land and forest degradation.

Tolerance/stress tolerance – the ability of an organism to maintain a degree of function or stability when exposed to a particular biotic or abiotic stressor, but not complete immunity (which is considered resistance).

Vulnerability – the degree to which a system, or part of a system, is susceptible to and unable to cope with a hazardous event, including climate variability and extremes.

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