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Plant ecological solutions to global food security Richard D Bardgett 1* and David J. Gibson 2 1 School of Earth and Environmental Sciences, The University of Manchester, Oxford Road, Manchester M13 9PT, UK. 2 Department of Plant Biology, Center for Ecology, Southern Illinois University Carbondale, Carbondale, IL 62901-6509, USA Summary 1. As global climate changes and the world population increases, agriculture faces an enormous challenge to increase food production in an equitable and sustainable manner. Principles and concepts derived directly from plant ecological research can help meet this challenge. 2. This series of 10 mini-reviews considers some of the key ways that plant ecologists can help inform and contribute to meeting this challenge. 3. The papers are grouped into three main themes of plant ecology, namely plant community diversity and structure, plant population dynamics and plant interactions, and plant-soil (belowground) interactions. 4. Synthesis: We identify a number of important knowledge gaps in areas where plant ecological 1

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Page 1: Plant ecological solutions to global food security file · Web viewEcosystem Services, Ecological Resilience, Food security, Sustainable Agriculture, ... Journal, such as plant community

Plant ecological solutions to global food security

Richard D Bardgett1* and David J. Gibson2

1School of Earth and Environmental Sciences, The University of Manchester, Oxford

Road, Manchester M13 9PT, UK.

2Department of Plant Biology, Center for Ecology, Southern Illinois University

Carbondale, Carbondale, IL 62901-6509, USA

Summary

1. As global climate changes and the world population increases, agriculture

faces an enormous challenge to increase food production in an equitable and

sustainable manner. Principles and concepts derived directly from plant

ecological research can help meet this challenge.

2. This series of 10 mini-reviews considers some of the key ways that plant

ecologists can help inform and contribute to meeting this challenge.

3. The papers are grouped into three main themes of plant ecology, namely plant

community diversity and structure, plant population dynamics and plant

interactions, and plant-soil (belowground) interactions.

4. Synthesis: We identify a number of important knowledge gaps in areas where

plant ecological research can contribute towards improving yield, nutrition,

ecosystem services, and environmental resilience of agricultural systems.

However, the adoption of plant ecological principles in sustainable agriculture

will require practical approaches to their implementation along with improved

understanding of social and economic barriers.

Key-words: Ecosystem Services, Ecological Resilience, Food security, Sustainable

Agriculture, Plant-soil interactions, Plant community dynamics, Plant-plant

interactions

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Introduction

Globally, agriculture is facing many challenges. Of paramount importance is the need

to increase food production to feed a burgeoning world population and to do this in a

sustainable way, reducing harmful effects of intensive agriculture on the environment.

But there is also a need for agriculture and the food industry to keep pace with shifts

in food consumption and to improve distribution and access to food. This challenge

also needs to done at a time of rapid environmental change, with rising temperatures

and extreme climate events threatening food production and placing considerable

pressures on the capacity of land to support crops and livestock. Further, the global

expansion and intensification of agriculture poses a significant threat to the

environment, causing habitat and biodiversity loss, water pollution, and increased

greenhouse gas emissions (Millennium Ecosystem Assessment 2005); and, in many

parts of the world, it is responsible for extensive degradation of soils, which

represents a major threat to both local and global food supplies (FAO 2015).

Together, these factors create a daunting challenge, which requires tackling various

constraints on crop production, but also many political and societal challenges to

ensure food supplies are safeguarded in an equitable and sustainable way, minimizing

harmful impacts on the environment (Foley et al. 2011).

Many solutions have been proposed to tackle this challenge, such as halting

agricultural expansion, shifting diets, increasing resource use efficiency of crops and

farm systems, closing yield gaps by harnessing the potential of underperforming

crops, and the production of food via sustainable intensification strategies (Foley et al.

2011; Godfray et al. 2010). Further, there are many social and political challenges that

need to be tackled in order to develop and implement sustainable food production

strategies, especially in developing countries where policies must include small

holders and less favoured groups (Austin et al. 2013). But how can plant ecology

contribute to this grand challenge? This challenge is what this Special Feature is

about: exploring promising and imaginative ways that the science of plant ecology

can contribute to the challenge of increasing food production in a sustainable way.

Plant ecological research in the Journal of Ecology has traditionally had, and

continues to have, a strong focus on fundamental research, often in more natural

settings. But this Special Feature recognizes that many of the dominant themes of the

Journal, such as plant community and population dynamics, plant-soil (belowground)

interactions, plant-plant, and plant-climate interactions, are of high relevance to

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modern agriculture. Further, as noted by Weiner (2017), this understanding in plant

ecology has now advanced to a level where we have much of the knowledge

necessary to build highly sustainable and resilient food production systems.

We have assembled a range of mini-reviews, which consider a variety of ways

that plant ecological knowledge could be used to inform agriculture and contribute to

the challenge of increasing food production in a sustainable way in both arable and

pastoral systems, and across different spatial scales. The papers cover a range of

perspectives on the application of fundamental ecological knowledge to sustainable

food production in crop and pastoral systems, including recent advances in

understanding of plant resource capture, plant-plant interactions, biodiversity-function

relationships, ecological resilience, plant defence, plant-soil (belowground)

interactions, and weed ecology. Here we provide a brief introduction to the Special

Feature. We first identify the dominant themes that are covered in the Special Feature

and then consider some of the challenges that we face in ensuring that such plant

ecological knowledge is effectively used to increase food production in a sustainable

way. We recognise that challenge of food security does not just concern food

production, in that it requires consideration of all aspects of the food system from

production to consumption (Erickson et al. 2008); But our focus here is mainly on

how plant ecological knowledge can contribute to this challenge, albeit in the context

of some of these wider challenges.

Plant community diversity and structure

The study of biodiversity-function relationships has long been a dominant theme of

plant ecology and the Journal of Ecology (Hutchings et al. 2012). Although a much

debated topic, there is a general consensus that biodiversity loss reduces most

ecosystem functions, and ecosystem multifunctionality, and impairs their stability

over time, and that functional traits of species have a major role in determining

diversity effects (Hector & Bagchi 2007; Cardinale et al. 2012). Most agro-

ecosystems, however, are monocultures receiving high inputs of agrochemicals, or

intensively managed, species-poor grasslands, and most agricultural lands have been

subject to considerable diversity loss (Newbold et al. 2015). As highlighted by Isbell

et al. (2017), attitudes are changing, and there is now growing interest in not just

preventing further biodiversity loss in agro-ecosystems, but also in their

diversification via increasing crop genetic diversity, mixed plantings, rotating crops,

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and diversifying field margins and surrounding landscapes. Further, as shown by

Isbell et al. (2017), strategically increasing plant diversity in agro-ecosystems has

multiple potential benefits, including increases in crop and forage yield, wood

production, yield stability, pollinators, weed and pest suppression, and soil health.

However, there are also many challenges in implementing diversification strategies,

such as the need for new harvesting equipment and to identify and maintain optimal

species mixtures to maximize yield and ecosystem services. But they argue that

overcoming these challenges is worthwhile and offer suggestions on how best to

implement appropriate diversification strategies.

Another topic that is receiving much attention is ecological resilience in the

context of global change (Oliver et al. 2015; Reyer et al., 2015). Recent studies

suggest that, in general, high plant diversity can stabilize ecosystem productivity and

services through increasing resistance to climate events (Isbell et al. 2015).

Agriculture in many parts of the world is threatened by more frequent extreme climate

events, such as heat waves, floods, and droughts, and diversification of agro-

ecosystems could help to enhance the resilience of food production systems to such

environmental perturbations. This issue is examined by Bullock et al. (2017), who

extend the ecological concept of resilience to agro-ecosystems in the context of

maintaining production of sufficient and nutritious food in the face of environmental

perturbations. They argue that resilience in agro-ecosystems manifests itself across

multiple spatial scales: at the field scale, for example, the use of mixtures of crop

varieties and forage species can enhance resilience; at the farm scale, resilience can be

increased by diversifying crops and livestock, and being flexible in the choice of crop

varieties in response to changing conditions; whereas at regional to global scales,

coordinated implementation of adaptive strategies across farms, along with

knowledge exchange to and among farmers, is required to create more resilient food

systems. Given this, they argue that achieving resilient food production systems

requires the merging of ecological and sociological approaches across multiple scales,

from the farm to the global scale.

Weiner (2017) also stresses the importance of biodiversity for sustainable crop

production, but in the context of crop rotations, which he argues is analogous to the

ecological concept of succession. As stressed by Weiner (2017), the choice of a crop,

or crops, within a rotation is one of the most important decisions a farmer can make:

the benefits of crop diversity in rotations for disease control, soil fertility, and crop

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yields, can be enormous, and are well documented in agriculture literature. But he

goes further, arguing that nothing demonstrates more the huge gap between

sustainability and modern agriculture than the restricted use of rotations, in terms of

both their length and the variety of crops used. The continuous cultivation of crops,

such as maize and wheat, requires enormous quantities of chemical inputs and, in the

longer term, can lead to significant soil degradation, which represents a major global

threat to food production. This degradation, coupled with the multiple potential

benefits of increasing the crop diversity across multiple scales (Bullock et al. 2017;

Isbell et al. 2017), adds support to the argument that diversification of cropping

system should be one of the highest priorities to increase agricultural sustainability

(Weiner 2017).

Plant population dynamics and plant interactions

Plant population ecology, including various forms of plant-organism interactions,

continues to be a key strength of Journal of Ecology. Included in this Special Feature

are four papers that emphasize in different ways how fundamental plant population

ecological research can inform agriculture. The issue of competition between crops

and ‘weeds’, and intraspecific interactions among crops, arose from agricultural work

over fifty years ago (de Wit 1960) and was brought into the realm of plant ecology by

John Harper and others (Harper 1976), which allowed many of the basic principles to

be worked out (Keddy 2015) and fed back into agricultural research (Tow and

Lazenby 2001; Zimdahl, 2004). The papers in this Special Feature touch on three

related topics: competition, phenological shifts in response to climate change, and

pollination services. Murphy et al. (2017) address kin selection and altruism in crops,

a topic first proposed as an Evolutionary Stable Strategy (ESS) among competing

soybeans (Glycine max) in Journal of Ecology (Gersani et al., 2001), although

regarded initially as controversial (e.g., Hess & De Kroon 2007; Semchenko et al.

2007). In their paper, Murphy et al. (2017) argue that reduced intraspecific

competition among crop plants, and hence higher stand yield, can be achieved through

artificial breeding programs that select for altruism, favouring cooperation among kin.

An analogous argument is proposed by Weiner (2017) who suggests that breeding

programs should not mimic natural selection but instead focus on increasing crop

yield at the expense of individual fitness. In a different proposal also based on the

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topic of competition, Gibson et al. (2017) review crop-weed competition and argue

that enhancements in crop quality (e.g., higher grain protein) as opposed to crop yield,

can be brought about through better understanding and manipulation of weed

taxonomic, phylogenetic, and functional trait diversity. Enhancement of food quality

through precision weed diversity control with less reliance on ‘clean fields’ would go

some way towards addressing global food quality concerns and sustainability.

Whatever advances can be made in food production through traditional

agricultural breeding programs, they have to be set in the reality of ongoing climate

change. Ecological research has a long history of teasing out the relevance of genetic

diversity of natural plant populations (Turesson 1930). On this theme, and using

phenology of wine grape cultivars as an example, Wolkovich et al., (2017) argue that

agricultural research on crops needs to follow ecological research on native plants to

document phenological diversity to help anticipate and meet the current climate

challenge. As the timing of climatic events changes (i.e., seasonality), only crops with

broad levels of phenological diversity will have a sufficiently wide gene pool to allow

selection to retain viable and sustainable crop populations.

Finally, an ecosystem service that scales up directly from plant-insect

interactions and is increasingly recognized as being important is that of pollination

services. In agricultural systems, insect pollinated crops rely heavily on non-native

honey bees (Apis mellifera), which are declining due to pest, pathogens, and

pesticides (Becher et al. 2013). Burke et al. (2017) discuss how ecological concepts

can be used to develop management practices to enhance pollinator services that will

in turn benefit both sustainable food production and wild-pollinator communities.

Encouraging the creation of native, wild pollinator communities will put less reliance

on the use non-native honey bees. Both Burke et al., (2017) and Gibson et al., (2017)

advocate management of agroecosystems based upon the application of community

assembly theory paying particular attention to metrics of functional trait diversity.

Plant-soil (belowground) interactions

Another dominant theme of plant ecology is plant-soil interactions and their

contribution to soil functioning and plant population and community dynamics. This

theme is also a focus in this Special Feature, with papers considering the importance

of plant-soil interactions for maintaining or enhancing soil fertility, and crop health

and agricultural sustainability. Soils in many parts of the world have been degraded

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by decades of continuous cultivation, overgrazing, excessive irrigation, and over

reliance on agrochemicals (FAO 2015). This degradation has led to increasing calls to

halt soil degradation, but also to devise sustainable ways of managing soils in order to

use resources, such as nutrients and water, more efficiently and reduce reliance on

fertilisers and agrochemicals.

As highlighted by Weiner (2017), soil organic matter is of central importance

to soil fertility; as such, a key feature of sustainable agricultural systems should be

high input of organic matter to soil as plant residues and animal wastes. However, the

functioning of soils is also strongly influenced by interactions between live plants,

their roots, and highly complex soil food webs. These rhizosphere interactions not

only regulate nutrient transformations and nutrient availability to plants, but also they

play a key role in plant defense, for instance via the recruitment and activation of

beneficial microorganisms that induce resistance or produce compounds that suppress

pathogens (Berendsen et al. 2012; Bardgett & van der Putten 2014). Further, these

rhizosphere interactions can promote other properties key to soil health, such as

carbon sequestration and stable aggregate formation, which improves the structure

and erosion resistance of soil (Rillig & Mummey 2006; Gould et al. 2016).

The diversity of organisms associated with plant roots is enormous, and, as

argued by De Vries & Wallenstein (2017), ecological interactions between plant roots

and microbial and faunal networks are critical determinants of soil function and plant

health. But they go a step further. Drawing on recent advances in understanding of

ecological networks, and growing evidence that plants can actually shape their

rhizosphere communities, they propose the ‘Rhizosphere Interactions for Sustainable

Agriculture’ (RISA) Model, in which crop roots recruit small, modular, highly

connected soil rhizosphere networks from large, static, relatively unconnected and

diverse bulk soil networks. Given that intensive agricultural practices typically disrupt

these belowground networks, they argue that a key feature of sustainable agricultural

systems should be to optimize connections between roots and rhizosphere food web

networks, and between rhizosphere and bulk soil networks. They propose avenues for

future research to achieve this and discuss how knowledge of belowground

connections can be applied in agricultural systems to sustainably produce food.

Perhaps the most intensively studied belowground interactions are symbiotic

associations between plants and soil microorganisms, which can stimulate plant

productivity by supplying growth-limiting nutrients to plants. The beneficial effects of

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nitrogen-fixing bacteria, which convert atmospheric nitrogen into ammonium

nitrogen, for crop yields are well documented, as is their ecological significance in

natural ecosystems (van der Heijden et al. 2008). But another important group of

symbionts that offer potential as a component of sustainable food production systems

are mycorrhizal fungi. In this Special Feature, Thirkell et al. (2017) explore how

ecological knowledge of arbuscular mycorrhzal fungi (AMF), which form symbiosis

with many agricultural crops, can inform on their role in agro-ecosystems. They

explore the direct beneficial effects of AMF symbiosis on crop performance and

yield, via improved nutrient uptake and diversification of nutrient sources acquired by

plants, and through non-nutritional effects, such as enhanced host tolerance to pests

and diseases, and competitiveness against weeds. They also highlight that the benefits

of AMF extend to the wider soil environment, in that extraradical hyphae serve to

bind soil particles together, thereby enhancing soil structure and resistance to erosion

(Rillig & Mummey 2006). High abundance of AMF has been linked to greater water-

holding capacity and the retention of nutrients in soil following rainfall events

(Bender et al. 2016). Importantly, however, they also stress that AMF colonization

can result in yield-reducing trade-offs, for instance through increased attractiveness

and nutritive quality of plants to herbivores, thereby improving herbivore

performance (Hartley & Gange, 2009; Koricheva et al., 2009). As such, they argue

that balancing these trade-offs should be a key component of any agricultural

management strategy involving AMF. Further, given that agricultural management, as

well as climate change, can cause significant shifts in the functioning of AMF, they

argue that to realize the benefits of AMF requires future research on AMF to be

carried out in real systems at the field, farm, and landscape scale.

Challenges and ways forward

As ecologists move forward to address questions fundamental to our discipline

(Sutherland et al. 2013), we are also poised to contribute and help solve applied,

societal issues. The papers in this Special Feature demonstrate that plant ecology in

particular can contribute in many ways to the challenge of increasing food production

in a sustainable manner (Fig. 1). But, as identified in all the papers, many hurdles and

constraints remain that need to be overcome to reap the benefits of plant ecological

knowledge in practical agriculture. Some of these challenges relate to future research

needs, whereas others to costs and benefits of ecological interventions, grower

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acceptance of new approaches, and the need to develop incentives and motivational

programs to encourage farmers to adopt ecology-based sustainable approaches. While

individual papers identify challenges and recommendations for integrating particular

aspects of plant ecology into sustainable agriculture, we highlight three major steps

that we believe need to be taken to fully realize the potential of plant ecological

approaches to contribute to the challenge of producing more food in a sustainable

way.

First, as identified by Wiener (2017), sustainable food production needs to be

placed as a primary goal of food production systems. As highlighted by others (e.g.,

Godfray et al. 2010), the goal of agriculture should not be to just maximize

production; rather it should optimize multiple benefits, including those to be gained

from plant ecology-based interventions considered here, which can bolster yields and

their nutritional value, but also wider ecosystem services and their resilience to

environmental change and extreme climate events. To achieve this, however, will

require transformational change in farm systems.

Second, while plant ecological knowledge can inform sustainable agriculture

now, important knowledge gaps remain. For instance, research is needed to optimize

mixtures and rotations for specific farm and environmental contexts, and to determine

how landscape-scale biodiversity influences ecosystem services and their resilience to

environmental change. This ecological research can help to identify sustainable

cropping systems (e.g., no-till agriculture) while planting genetically modified,

herbicide-tolerant (GMO) crops (Gibson et al. 2015), and in the context of the

evolution of herbicide-resistant weeds (Gage et al. 2015; Owen et al. 2015). Also,

there is a need for improved understanding of the scaling of ecological processes

across highly fragmented agricultural landscapes, and for greater knowledge of the

mechanisms by which root-microbial interactions influence nutrient supply and plant

defence in different agricultural settings, including those challenged by nutrient poor

soils. We also need to better harness evolutionary processes in crop breeding

programs and identify traits that not only relate to yield and nutritional quality, but

also have wider benefits, for instance for soil health.

Finally, to fully reap the benefits of plant ecology-based interventions in

sustainable agriculture will require practical approaches to their implementation to be

developed and deployed, which requires translational research and engagement with

farmers, policy makers, breeders, and agricultural scientists. Further, these approaches

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will not only rely on improved understanding of social and economic constraints to

the adoption of new ecology-based approaches, and of their costs and benefits, but

also educational and motivational programs to encourage farmers to adopt new

approaches. We very much hope that you enjoy reading the papers in this Special

Feature of Journal of Ecology, which highlight the many and varied ways that plant

ecological knowledge can contribute to the global challenge of producing food in a

sustainable way.

Acknowledgements

We are grateful to all the authors of this Special Feature for their contributions and to

James Ross for his help in putting it together.

Data Accessibility

This paper has no data

Author Contributions

RDB and DJG jointly conceived and wrote the paper

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Fig. 1. Schematic illustrating some of the main ways discussed in this Special Feature

that plant ecology can contribute to sustainable food production. (Photo credit

Bryan Young: US soybean (Glycine max) field infested with the weed

waterhemp (Amaranthus tuberculatus)).

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