Concepts of trait diversity – the key to effective IPM for resilience in arable systems?

Abstract

Modern agriculture is perceived to be unsustainable having pursued a high productivity, reductionist approach for many decades. The solution proposed for restoring ‘sustainability’ is often encapsulated in the term ‘diversity’ but this is frequently as ill-defined and open to wide interpretation as the word sustainable. Key to determining whether diversity is ‘the answer’ is defining what diversity means in practice in the field. We attempt to describe the concepts and components of diversity and, crucially, how they might combine and interact in agricultural systems. The key concepts are: (1) complexity, (2) variation, and (3) spatio-temporal interaction, with the latter comprising (a) heterogeneity, (b) spatial connectivity, and (c) temporal connectivity. We suggest that this might lead to new strategies of diversity deployment and an index of resilience, a key ingredient of sustainability. These measures of diversity are explored in the context of crop resistance to pests and pathogens and the potential to maximise the benefits for integrated pest management in arable crops.

Keywords

Diversity connectivity complexity IPM variation spatio-temporal interaction heterogeneity crop protection intercropping sustainability low inputs

Managing agricultural diversity and heterogeneity

The driving forces in modern agriculture since the ‘green revolution’ have centred on mechanisation, agrochemical inputs, and a shift towards commodity crops to increase crop productivity (Frison, 2016). This ‘industrialisation’ of agriculture has created significant improvements in crop yield, but has occurred at the expense of diversity: crops are grown as monocultures of single crop genotypes, farms tend to specialise on specific crop types, and landscapes become dominated by one or a few agricultural land uses, with little native vegetation. Alongside this, the trend towards homogeneity has favoured a predominantly reductionist approach to modern crop breeding (e.g. Kiær et al., 2022), which assumes that the desirable traits for enhanced crop performance can be assembled in single, optimised genotypes to meet the goals of crop quantity, uniformity and consistency valued by processors and other end users. While this approach combines much functional diversity from many sources in a cultivar's pedigree and has led to highly productive modern cropping systems, the lack of diversity across scales, from crops to value chains, has created vulnerabilities in food systems that become particularly apparent during periods of external stress (Khoury et al., 2014; Mahaut et al., 2021). The biological functions supporting productivity are increasingly provided through external inputs, crop breeding has focussed on a small number of highly competitive resource-hungry species, and system resilience has been effectively outsourced to the agri-input industries, particularly for pesticides and fertilisers.

This approach fails to maximise the use of diversity in crop production, even though it is a cornerstone of integrated pest management (IPM): diversity in the crop and soil substrate underpins diversity in plant resistance or apparency to pests, while spatial and temporal diversity of organisms at field, farm and landscape scales can influence the abundance and diversity of pests and their natural enemies (Haan et al., 2020; Stenberg, 2017; Wyckhuys et al., 2022). By harnessing complementary spatial and temporal interactions between plant types expressing different suites of traits, crop productivity and pest and disease control could be improved through processes of niche differentiation or facilitation (Brooker et al., 2021; Homulle et al., 2022), and with potential to increase resilience to stress through improved yield stability (e.g. Weih et al., 2021) or via the insurance effect (e.g. Yachi and Loreau, 1999). Indeed, biodiverse systems are more productive (Brooker et al., 2016) and even small increases in biodiversity can lead to disproportionate increases in function (Cardinale et al., 2012). Evidence of this association between diversity and productivity comes from a wide range of production systems and scales (Davis et al., 2012; Egli et al., 2021; Smith et al., 2023; Renard and Tilman, 2019). But what level of diversity is needed to reap the benefits of improved crop system functioning? The conceptual basis of calibrating trait diversity – that is, which components should be included and how many components is optimal – is not well established for crop systems. There is clear need to define and understand diversity as the ecological basis of IPM to support a shift away from the still-dominant regime of chemical-based crop protection (Deguine et al., 2021).

Here, we address these questions at the scale of the crop (i.e. field scale) to ascertain the degree of spatial and temporal diversity in crop traits that leads to more effective IPM and increased resilience, both to environmental stress and to variabilities in agri-input supply chains. Understanding how much diversity is needed, and how it should be deployed in the field, is a crucial first step in defining the traits that maximise the benefits of inter-specific and intra-specific crop diversity for the purposes of crop breeding and crop agronomy.

Context and concepts of diversity

The recent spike in the cost of agricultural inputs, particularly nitrogen fertiliser, has highlighted how our reductionist approach to crop production is highly dependent on costly inputs, or, conversely, it lacks resilience without such inputs. Furthermore, high input levels required to deliver expected levels of crop productivity are intimately associated with lack of trait diversity. Clearly our cropping systems need to be more resilient to function under lower inputs when required and there is great potential in taking this direction as increased resilience is thought to be functionally associated with increased diversity (Yachi and Loreau, 1999). But what is the ‘diversity’ being referenced in these relationships? Do we know which and how many traits need to be diverse? Do we know what range of differences is needed for each trait or trait aggregation? Can we calibrate ‘diversity’ so that we can design more functional cropping systems that are less dependent on inputs?

The term diversity itself has many synonyms such as: variety, miscellany, assortment, mixture, range, array, multiplicity, variation, heterogeneity, difference or distinctiveness; these terms effectively describe particular concepts of diversity. Here, we consider the fundamental concepts of diversity to comprise (i) complexity: the number of components and (ii) variation: the nature of the difference between components and the size or magnitude of that difference. In practical application, these concepts are of minimal use without describing their spatial and temporal dimension of deployment as it is only in their spatial and temporal context that the combined functionality of diversity concepts become relevant. We consider a combination of heterogeneity and connectivity in time and space to describe the spatio-temporal interaction of these concepts.

Implementation context of diversity

We will consider the application of diversity in the context of resilience of arable crops to climate change and pests and pathogens. Essentially the context is as part of Integrated Pest (/Crop) Management or IPM (/ICM). ‘Diversification’ in resistance breeding has often been proposed as an important factor for controlling pest and pathogen spread and the absence of diversity in resistance genes in wheat crops worldwide has had devastating consequences: for example, in the United States in the early 1930s and 1950s, and even recent years, wheat yields have been compromised by resistance-breaking UG99 races of stem rust spreading from Africa (Ellis et al., 2014). Such epidemics were associated with changes in the population of the stem rust fungus, which enabled it to overcome genetic resistance of common wheat varieties. Diversity in plant resistance traits is equally applicable to arthropod pests, whether to tackle resistance-breaking biotypes (e.g. Russian Wheat Aphid: Bapela and Tolmay, 2021; potato cyst nematode: Beniers et al., 2019) or combat the damaging effects of multiple pest species (e.g. of cereals or potato: Crespo-Herrera et al., 2019; Gartner et al., 2021). The strategy for deploying diversity in pest and pathogen resistance traits, whether race-specific or species-specific genes or other traits, is critical for ensuring its efficacy in practice.

The examples given above indicate that diversity is needed in the form of more or different sources of pest or pathogen resistance, which might traditionally involve different resistance specificity genes, different categories of resistance such as ‘major gene’ and ‘minor gene’, polygenic resistance where each gene has a smaller effect that together are often characterised as ‘partial’ or ‘field’ resistance (Walters et al., 2012) or traits that lead to improved pest tolerance (Mitchell et al., 2016). Furthermore, resistance traits may be expressed temporally, for example as ‘seedling’ or ‘adult plant’ resistance, where the genetic and molecular mechanisms involved might vary considerably (e.g. see a review of mechanisms of ‘mature plant resistance’: Develey-Riviere and Galiana, 2007). Other traits that may affect resistance expression, or indirectly lead to resistance, such as nutritional quality, resource capture, and other forms of plant chemical and physical defence (Mitchell et al., 2016) are often not considered in plant breeding programmes for single gene resistance. Equally, spatial and temporal deployment of resistance trait diversity is often not taken into account. If trait diversity is to deliver its full potential for resilience in crop production, whether to pathogens, arthropod pests or other external stresses, then the component mechanisms and concepts concealed within the ‘black box’ use of the term ‘diversity’ should be evaluated, calibrated, and a strategy for their exploitation developed. Next, we will define and illustrate the main concepts underpinning the functionality of diversity in crop traits and how it can be applied practically in IPM/ICM.

Calibrating the concepts of diversity

It is necessary to define the concepts of diversity to manage or design systems for their optimisation in practice. Furthermore, the culmination of multiple types of diversity may have additive, synergistic or even antagonistic effects on resilience outcomes. To calibrate the categories of diversity outlined above – variation, complexity, spatio-temporal interaction – in ways that taken into account both the functionality of diversity and how it might be managed in a field setting, we provide the following definitions:

Some simple definitions of ‘diversity’ constituents:

Complexity: number of components

Variation: type and magnitude of physical or molecular differences between the components

Spatio-temporal interaction: linkage or interaction between the components

Heterogeneity: irregularity of patch shape (and size) of the components

Spatial connectivity: proximity of the patches of components or degree of mixing

Temporal connectivity: timing and duration of interaction of the components

Diagrammatic examples of spatio-temporal interaction types are shown in Figure 1. For each of these diversity measures we suggest a 1 to 4 conceptual scale from weak to strong expression as described in Table 1. The spatio-temporal dimension is calculated as the mean of its three component concepts (a, b and c) and the overall score is the sum of the mean values (1, 2 and 3) representing a resilience score that can be categorised as low, medium, high or very high. Hypothetical examples are given in Table 2 to show that there are a number of ways to achieve different resilience categories. The resilience score assumes additive effects of combining diversity concepts, although in practice there might be synergistic (more than additive) or detrimental (less than additive) outcomes of their combinations. It will be important to identify which molecular and/or physical mechanisms combine to give synergistic, additive or detrimental outcomes, as this should lead to better understanding of ways to optimise diversity in crop systems, that is, which types of diversity to prioritise to achieve optimum outcomes. This is particularly important when considering the practicality of implementing diversity in field conditions in terms of sowing, managing and harvesting a mixed crop. A major barrier to uptake of crop diversification strategies is lack of appropriate knowledge amongst farmers and the perceived risks and uncertainties of diversifying (Brannan et al., 2023). We assumed, therefore, that a more diverse crop will be perceived as more complex to manage, even if this might not be the case in practice (Table 1).

Figure 1.

Diagrammatic examples of spatio-temporal interaction types.

Table 1.

Diversity parameter scale descriptions.

Table 2.

Hypothetical examples of diversity calibration and resilience estimation.

Examples of diversity concepts

Below we review some examples of the effects of different diversity concepts on pest and pathogen control and yield in arable crops. These represent some of the evidence base that contribute to the framework described above.

Complexity: Number of components

There are many examples of where increasing component numbers both reduces pest abundance or disease incidence aboveground and belowground and increases yield (Gardarin et al., 2022; Gu et al., 2021, Homulle et al., 2022, Iverson et al., 2014; Kølster et al., 1989; Mundt, 1994; Nitzsche and Hesselbach, 1983; Smithson and Lenne, 1996), as clear illustrations of the classical biodiversity-ecosystem function curve (Cardinale et al., 2012). This is shown very clearly in reduced Rhynchosporium infection in winter barley which is directly proportional to the number of components in the mixture, and greater component number leads to yield increase even in the absence of disease (Newton et al., 1997). Similarly, aphid abundance was lower in wheat cultivar mixtures, with no yield impairment (Duan et al., 2022). However, a small amount of particular varieties in an intra-specific mixture of plants can contribute a disproportionately large effect on the function of the mixture for some outcomes such as disease reduction (Newton and Skelsey, 2023), so the nature of such responses is likely to be trait specific. Experimental work is needed to examine whether this phenomenon exists when the number of crop species increases. This is not confined to annual crops as in trees this same concept works, revealing that up to 20 components can be beneficial (Huhn, 1985, 1986a, 1986b).

Variation: Type and magnitude of physical or molecular differences between the components

The ordinal diversity concept scales described above have no units as they need to be applied across many differing traits. For any given ‘crop’ the diversity in pest or pathogen resistance may be at the level of different single resistance genes such as isogenic lines differing only in specificity towards a pathogen race, through to mixtures of cultivars showing different degrees of trait expression (Zhan et al., 2008), to different traits within or between genotypes (e.g. leaf trichome presence, phloem composition and defensive signalling affecting cereal aphid infestation of barley: Leybourne et al., 2019), and to strongly contrasting trait combinations used in inter-species mixtures or intercrops (Altieri, 1991). Changing these component dynamics at any level may have implications for the dynamics at other levels with unforeseen consequences. For example, incorporation of a different crop species may change the physico-chemical environment, in terms of air movement, humidity, temperature and apparency, and thereby alter the risk of pests or pathogens encountering or being able to infest/infect their host. Furthermore, we use terms such as ‘pest’ and ‘pathogen’ but these refer to the outcome of the interaction between organisms such as a plant and a bacteria or a fungus under a particular set of circumstances when the microbe causes damage. However, such circumstances could be considered exceptional, or at least not the norm, because at other times the microbe may function as a beneficial or mutualistic organism. Management of diversity could potentially favour maintaining organism interactions in benign or mutualistic states (Collinge et al., 2022; Newton et al., 2010b), or preventing dominance of a virulent pest/pathogen type (e.g. pesticide-resistant strains) and therefore we need to understand the fundamental attributes of the crop as an agro-ecosystem that will favour this outcome; it is likely that diversity is central to these attributes. It is important to note that traits contributing to improved pest and pathogen control include those acting indirectly to increase plant nutrition and vigour: for example, wheat variety mixtures show greater resource use efficiency and yield (Kristoffersen et al., 2022), while also stabilising selection for fungicide resistance (Kristoffersen et al., 2020) thereby enhancing IPM.

Extending the concepts of functional state of specific organisms to environments, soils are already highly complex ecosystems that are difficult to reduce to specific parameters but have major impacts on plant health and the aboveground environment also, even suppressing aboveground insect pests through chemical changes in the plants (Pineda et al., 2017). Soils can themselves be ‘suppressive’ for plant disease but their functional status can be strongly impacted by both the type and diversity of the plants growing in them. For example, different species directly affect the growth of the following crop species growing in the same soil (Hannula et al., 2020) and mixing soils from mono-specific sources works synergistically for disease control (Ma et al., 2018). However, within the complex of the soil microbial community, key species such as mycorrhizae and Induced Systemic Resistance (ISR) eliciting rhizobacteria can have strong disease-controlling effects (Cameron et al., 2013).

Spatio-temporal interaction: Linkage or interaction between the components

Heterogeneity: Irregularity of patch shape (and size) of the components

The length or volume of the interface between patches of different plant types (i.e. with different resistance traits) is crucial to their ability to interact and this is defined by the patch shape. For example, a circular patch minimises the edge effects with the adjacent component compared with an irregular patch shape. Often parameterised as perimeter-area ratios, this is identified as a key factor in connecting habitats of pests and natural enemies across landscapes (Bianchi et al., 2006; Díaz-Forestier et al., 2021; Jones et al., 2021).

Spatial connectivity: Patch size of the components

Where diversity is deployed such as in cultivar mixtures, it is often assumed that components must be homogeneously mixed, and models made to support development of mixtures efficacy often confirm this assumption (Goleniewski and Newton, 1994). Ecological models that seek to explain refuges in pest–host interactions show the importance of connectivity and patch size (Holyoak, 2008). Pathogens have differential dispersal gradients so some similar considerations may apply. However, rather than test this out in models where every process and assumption might need to be justified and interpreted, this was tested in the field with commercial agricultural machinery. This quickly and reproducibly demonstrated that heterogeneous mixing of component cultivars gave larger increases in yield and reductions in disease than homogeneous mixtures (Newton and Guy, 2009). Indeed, the areas with the most irregular patchiness were most effective, likely mimicking effects observed in natural vegetation. Further research is needed using this approach to understand the effects of host plant connectivity in crop mixtures on arthropod pests, which are likely to respond to patch size according to life history processes and mortality risks (e.g. Olson and Andow, 2008).

Spatial connectivity is the basis of disease control diversification schemes for crop cultivars at a farm scale such as yellow rust on wheat or mildew on barley (UKCPVS, 2007) but is important also right up to a global scale where understanding the risk can facilitate choice of mitigation strategies (Xing et al., 2020).

Temporal connectivity: Time and duration of interaction of the components

To introduce diversity in temporal concepts can be difficult in practice but is carried out in relay intercropping (Brooker et al., 2015; Homulle et al., 2022). Under-sowing with grass or clover is often practiced in arable crops allowing the understorey to flourish when the main crop matures or is harvested. Using strip cultivation or sowing and specialist harvesting machinery, it is possible to intercalate crops with very different sowing, agronomic and harvesting requirements to make better use of both aboveground and belowground resources. A mixed crop such as cereal species and broad leaf dicots can be differentially treated with herbicides to remove a component not required for harvest but still contributing to the harvested component's productivity or longer-term soil health gains.

Temporal diversity can, however, have potential negative implications for pest and pathogen control. Extended periods of ground cover (e.g. in relay intercrops or overwinter cover crops) can act as green bridges between crop growing seasons, providing a resource that keeps pest and pathogen populations ‘ticking-over’ and thereby facilitating more rapid infection or colonisation in subsequent crops (Huss et al., 2022). However, host plant diversity can play an important role in reducing such green-bridge phenomena both for the immediate crop (reviewed in Gardarin et al., 2022) and long-term pest or pathogen population management. An example of the latter is deployment of different resistance genes in winter and spring varieties of the same crop species. The mlo powdery mildew resistance gene is not deployed commercially in winter barley germplasm and may have contributed to the durability of this gene's efficacy in spring barley germplasm despite its near fixture in current elite cultivars (Kusch and Panstruga, 2017; Lyngkjær et al., 2000).

Implementation: Enhancing resilience scores by application in integrated pest/crop management

IPM is defined as ‘the careful consideration of all available pest control techniques and subsequent integration of appropriate measures that discourage the development of pest populations and keep pesticides and other interventions to levels that are economically justified and reduce or minimise risks to human health and the environment. IPM emphasises the growth of a healthy crop with the least possible disruption to agro-ecosystems and encourages natural pest control mechanisms’; or more succinctly: ‘Integrated Pest Management (IPM) is an ecosystem approach to crop production and protection that combines different management strategies and practices to grow healthy crops and minimise the use of pesticides’ (FAO, 2018). It is a multi-component approach, but it also capitalises on diversity in each of the components. To be effective it should also be implemented across all scales from single plant to global. However, different IPM options are best optimised at different scales, so phytosanitation assumes greater importance at large scales whereas pesticides need to be optimised at a fine scale (Newton et al., 2011). Crop diversity can be deployed across all scales, ranging from landscape-level diversity in field size and crop composition to reduce pest and pathogen pressures (Haan et al., 2020), to temporal rotation of crops within a single field to avoid build-up of soil-borne pests (e.g. Jing et al., 2022), to inter-species and intra-species crop diversity within and between fields using intercrops and cultivar mixtures with different resistance genes (discussed above). Different types of research, advisory/extension, knowledge exchange and regulation organisations and authorities are relevant to inform, advise and encourage effective implementation of diversity at relevant scales (Newton et al., 2011).

An approach to optimising IPM might be to consider all the options available with respect to their effect on risk enhancement or mitigation. Each option should be considered in terms of its likelihood probability and feasibility of manipulation (Chakraborty and Newton, 2011). Such analysis will help choose and prioritise the options available. However, the area where effective knowledge is limiting is the interaction of these components: which are additive, synergistic or antagonistic? For example, one of the three principles that make cultivar mixtures effective against highly specific biotrophic pathogens, such as the rusts and powdery mildews, is induced resistance (Chin and Wolfe, 1984). Therefore, utilising resistance elicitors in these circumstances could be counter-productive as this component would already be triggered and therefore be ineffective (Finckh et al., 2000). Likewise, introducing diversity into the components of crop protection product application programmes, especially those involving elicitors (Yassin et al., 2021), needs an understanding of how the components interact and whether additive, synergistic or antagonistic outcomes result. More development of aids to support IPM decisions is needed that effectively integrate the available knowledge, especially with that of the practitioner. However, the broad concepts of diversity in terms of complexity, variation and spatio-temporal interaction dimension are already reflected in IPM principles, albeit not explicitly considered overall.

In summary, diversity has potential to enhance IPM through a multitude of tools that build upon the key concepts of complexity, variation and spatio-temporal interaction in the whole crop system. Multiple components of diversity are desirable taking care to ensure interactions are additive or synergistic within and between diversity concepts, but effort needs to be invested in translating these principles into practical management advice. Here, we have focussed on how diversity might be deployed in the crop to improve pest and disease control. An important next step is to consider how this diversity should be tailored to functional traits of pests and pathogens, which affect their survival, dispersal, host range, life cycle characteristics (e.g. diapause/hibernation) or ability to generate survival structures. A strong example is the effect of facultative endosymbionts of sap-feeding insect pests, which have been shown to affect pest fitness characteristics including host plant range, fecundity and susceptibility to natural enemies (see review by Zytynska et al., 2021).

Future steps: The known unknowns

The current domination of agriculture by monocultures of arable crops is increasingly cited as a cause of many ecological issues of concern such as the decline in the abundance and diversity of insect pollinators (Brooker et al., 2015; Sánchez-Bayo and Wyckhuys, 2019). Whilst this may be credible, the solution will not be simply increasing diversity per se. Historically, agricultural practice was more diverse but it was effective in historic contexts which might not translate to current homogeneous industrial food production environments (IPES-Food, 2016). Much else has changed in the semi-natural and cultivated environment as well as the socio-economic and political world since ‘the good old days’. If diversity is a key to solving these big agro-ecological issues, then we must understand all the components of its functionality to restore sustainability and resilience into our arable cropping systems. However, monocultures as mono-specific stands, rather than pure stands of a single genotype, were used historically and still are in farmer small holdings in less-developed countries and express diversity as landraces associated with increased functional resilience (Newton et al., 2010a).

Crops can be grown in hydroponic systems where it is assumed (sometimes incorrectly) that the only organisms are the plants, but this requires a very high level of control over the environment and a high level of management. However, out in the field where there is much less control over the environment, crop production is about management of highly complex interactions between multiple organisms, the crop plant being just one. Here the plant and soil microbiomes are another level of diversity not considered in detail in this article as we are at early discovery stages of their function and dynamics. Nevertheless, there is evidence that microbiome diversity is influenced by other dimensions of diversity (Burrows and Pfleger, 2002; Dang et al., 2020, Li and Wu, 2020) and system function is dependent on the nature and number of interactions between all the component organisms. Indeed, others have presented a conceptual framework for plant–soil feedback that develops ecological concepts of diversity in an agricultural context (Mariotte et al., 2018). Further understanding may be derived from integrating such frameworks with the diversity-calibrated resilience concepts outlined here.

In analysis of the structure of quantitative plant–parasite interactions, Moury et al. (2021) found that correlations between the efficiency and range or scope of the resistance of plant genotypes, and between the host range breadth and pathogenicity level of parasite strains, were overall positive. They concluded that this called into question the efficiency of strategies based on the deployment of several genetically differentiated cultivars of a given crop species in the case of quantitative plant immunity. This was based on a limited number of datasets investigated for correlation of nestedness and modularity with host range and illustrates the highly complex nature not only individual host–pathogen interactions, but also the compounding effects of diversity deployment. These concepts should find their utility in hypothesis testing in such explanatory models but also to guide practical deployment.

At a basic level the interaction between all organisms in an IPM context is defined by physical and chemical or molecular interaction between pest or pathogen and host and between effectors and receptors (Toruño et al., 2016). At a higher level it is potentially the complex sum of many such recognition events perhaps best seen as trophic interactions as essentially it reduces to resource capture and utilisation. However, these interactions may be optimised at the level of an individual or a community. Signalling of all types occurs within and between individuals and within and between species, that is, at all levels. System sustainability and resilience is therefore explained by a complex of organism interactions also in all parts and at all levels. These signals drive the high level or functionally defined ecological interactions of competition and complementarity. Understanding which interactions (type, level or specificity) drive the system and how can they be perturbed or manipulated for enhanced resilience and productivity is the key to addressing issues raised for plant productivity and disease control in the context of climate change and food security. Understanding diversity requires bringing together fundamental understanding of molecular signalling with whole systems design at field, farm and landscape scales, and concepts that may be parameterised across all levels.

Footnotes

Acknowledgements

We thank particularly the Aspen Global Change Institute for stimulating thinking our thinking at the ‘Food System Impacts of Pests & Pathogens in a Changing Climate’ in August 2019 which helped bring these ideas together. We also thank the Scottish Government Rural and Environment Science and Analytical Services (RESAS) Strategic Research Programme (2022–2027) funding to the James Hutton Institute.

Declaration of conflicting interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

ORCID iD

Adrian C Newton

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