# Cultivate biodiversity to harvest food security and sustainability

Delphine Renard, David Tilman

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## To cite this version:

Delphine Renard, David Tilman. Cultivate biodiversity to harvest food security and sustainability. Current Biology, 2021, 31 (19), pp.R1154-R1158. 10.1016/j.cub.2021.06.082. hal-04910412

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1 Cultivate biodiversity to harvest food security and sustainability

2

3 Renard Delphine¹*, Tilman David²,³.

4 ¹ CEFE, Univ Montpellier, CNRS, EPHE, IRD, Montpellier, France

5

6 ² Bren School of Environmental Science and Management, University of California Santa

7 Barbara, California 93106, USA

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9 ³ Department of Ecology, Evolution and Behavior, University of Minnesota, St Paul,

10 12 Minnesota 55108, USA

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12 * [delphinerenard@hotmail.fr](mailto:delphinerenard@hotmail.fr)

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14 Abstract

15 A confluence of discoveries in ecology and agriculture suggests that biodiversity can help
16 address the sustainability problems facing modern intensive agriculture. Here we explore
17 several questions related to this possibility. Can increases in national crop diversity help
18 increase the stability and security of national food systems? Can practices based on greater
19 crop biodiversity produce yields that compete with the yields of the long-standing high-input
20 monoculture model? What are the appropriate levels and combination of crops to be used? In
21 this essay, we highlight recent research that suggests it is time to begin unlocking the
22 agricultural potential of greater biodiversity from the level of crop genetic diversity to new
23 crops, and to do so on spatial scales from individual fields to nations. Recent research
24 suggests that the result may be greater and more stable yields, lower land clearing and lower
25 use of agrochemicals and the harm they can cause.

26 Context

27 Evolution led to the formation of ~380,000 species of vascular plants on earth [1]. This
28 diversity is not surprising given the global heterogeneity of earth's soils, climate and
29 topography and the different plant traits needed to deal with various aspects of this
30 heterogeneity. Of these species, ~6,000 have been used as sources of human food [2], but just
31 4 species - wheat, rice, maize and soybeans - provide 70% of the calories we consume. It
32 seems ironic that, on a planet where natural selection led to such amazing plant diversity,
33 human selection has favored so few crop species and has cultivated them ubiquitously [3].

34 Perhaps because modern agriculture relies so heavily on a few crop species, the success of
35 these crops is highly dependent on their genetic biodiversity [4]. Consider some Green
36 Revolution crops, such as rice. Continual breeding efforts have become necessary to retain its
37 high yields in the face of rapidly evolving fungal, viral and bacterial diseases and unfavorable
38 climate conditions [5]. Genetic biodiversity is the basic raw material needed when breeding a
39 new variety of a crop, whether it is developed to increase yield, nutritional quality, to make it
40 more resistant to emerging pests and diseases, or to allow it to grow in warmer, cooler, drier
41 or wetter conditions [6]. Maintaining this within-species biodiversity is so important that
42 special facilities like seed banks and botanical gardens are dedicated to conserve a large
43 number of distinct varieties of all of the major crops and their wild ancestors. For instance,

44 more than 125,000 varieties of wheat in total are held in various collections, such as the US

45 Department of Agriculture National Plant Germplasm System. The Biodiversity Convention

46 also gave a clear mandate for on-farm conservation of landraces, a key to subsistence farming

47 systems that provide 30-34% of the world's food [7].

48 As the global human population grows from 8 to over 10 billion people, and as more people

49 shift their diets towards higher consumption of meats and calories [8], agriculture faces

50 immense challenges. It will need to double global crop production to meet food demand and

51 to overcome persistent malnutrition, at the same time that it greatly decreases its global

52 greenhouse gas emissions (over 30% of the global total, [9]), water and air pollution, land

53 degradation, and destruction of natural ecosystems.

54 Against this agricultural backdrop, evidence suggests that some of these challenges could be

55 addressed by an appropriate use of biodiversity, including greater genetic and species

56 diversity. Consider the results of the past quarter century of ecological and agricultural

57 research. They have demonstrated that Earth's natural and managed ecosystems are more

58 productive and sustainable, and less susceptible to climate hazards and to disease outbreaks

59 when they have greater plant biodiversity [10–16]. Although these may seem like bold

60 assertions, they are based on hundreds field experiments in both ecological and agricultural

61 realms and a multitude of resulting peer-reviewed publications.

62 Below, we suggest three major ways that increases in crop biodiversity could help make food

63 production be more secure and stable, lower environmental harm and support human health.

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## 1. National crop diversity for food stability and security

67 Climate change poses a major threat to food security. Climate events, especially droughts,

68 have caused 50% of the observed sudden drops in national food production since the 1960s'

69 [17]. Crop failures destabilize national and global agricultural markets, cause food prices to

70 rapidly rise, harming access to food, especially for the world's poorest people. Because

71 droughts, heat waves and other climate extremes are expected to become more frequent and

72 intense in the future, the frequency of shocks to the global food supply system may increase.

73 Nations could somewhat address this issue with sufficient water resources and adequate

74 irrigation infrastructure, or with access and adoption of crops that are more resistant to

75 drought and higher temperatures. However, the increasing scarcity of usable water and the

76 difficulty of breeding for higher yields under an erratic climate [18] call for complementary

77 solutions to build more robust agricultural systems.

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79 The use of greater crop diversity within a country has the potential to markedly increase the

80 year-to-year stability, security and reliability of its food supply [19]. Analyzing 50 years of

81 data across 91 nations, Renard and Tilman (2019) found, for instance, that countries with a

82 crop diversity of 4 had severe crop harvest declines about once every 7 years, while those

83 countries with crop diversity of 10 had such declines only about once every 60 years (Fig. 1).

84 This stabilizing effect of crop species diversity is explained by what is called the portfolio or

85 insurance effect [19,20]. Because different crop species exhibit different responses to hot,

86 cold, wet or dry weather, and to pests or diseases, greater crop diversity is better at buffering

87 out the impact of environmental variation on the total harvest of all crops in a country.

88
<figure><img src="image_3.png" /><figcaption>**Figure 1.** Relationship between the national effective crop species diversity and the probability of losing 10%, 15% and up to 25% of national harvest. Using FAOSTAT data, the 91 nations studied in Renard and Tilman (2019) were equally divided into five classes of crop diversity (average diversity of each class: 4, 6, 8, 10, 15). For all nations in each diversity class, we calculated the probability of harvest loss using the method described in Renard and Tilman (2019). Crop diversity is not a mere count of crop species, but depends on their abundances. It is measured using H', the Shannon diversity index, and expressed as $e^H$.</figcaption></figure>

In this study, crop diversity had the greatest stabilizing effect of all factors examined (Fig. 2). Irrigation was of next greatest importance while fertilization showed no significant effect on stability. As would be expected, greater year-to-year variation in rainfall and growing season temperature decreased the stability of total national crop harvests. These results suggest that for many countries, increases in national crop species diversity could significantly promote the year-to-year stability of the total food harvest in a nation in the face of current and likely increasing climatic variability, without a cost to mean yield [19,20].

Importantly, merely planting more rare crops offers little if any stabilizing benefits. To attain the benefits of higher crop diversity, diversity must be increased so as to have more crops that each contributes importantly and about equally to national food production. Future research will need to identify those crops that maximize the portfolio effect under a changing climate for particular nations and their climatic and soil conditions. If those crops could also be nutritionally diverse, appropriate diversification within nations could also better fulfill dietary needs [21]. Minor or underutilized crops worldwide represent a still untapped source of diversity to meet both ends. Consider quinoa. This traditional Andean crop was cultivated by only three nations in the 1960's. Thanks to the promotion of its nutritional qualities and robustness to climate, 95 nations worldwide are now cultivating or testing their ability to grow quinoa, including the UK, Denmark, Tibet, India, The Netherlands, China, Brazil and Cuba [22].

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<figure><img src="image_4.png" /><figcaption>**Figure 2.** Main determinants of national, caloric yield stability. Bars with a positive value correspond to a stabilizing effect (crop species diversity, irrigation and fertilization), and bars with negative values reflect a destabilizing effect (precipitation and temperature temporal instability). Stars indicate factors that significantly affect yield stability. In all cases, *** means P<0.001. Lack of * means P>0.05. Figure produced using results from [19].</figcaption></figure>

**2. Crop diversity within fields for higher yields and lower environmental harm**

In some of the world's breadbaskets, the maximal yields of major crops, like wheat and rice, have reached plateaus that crop geneticists and agronomist have not been able to exceed for a decade or longer [23]. In such cases, it might seem that the only way to increase food production would be to clear more land. Land clearing, though, already releases globally significant amounts of carbon dioxide and is the major cause of biodiversity extinction risks globally [24]. However, a modern twist on an ancient agricultural technology, intercropping, may provide an environmentally and economically beneficial alternative to additional land clearing.

Intercropping entails the cultivation of two or more spatially intermingled crops species on the same piece of land. Numerous well-controlled and well-replicated experiments conducted worldwide show that intercropping produces from about 16% to 30% greater yields on a given piece of land than do each crop species cultivated in monoculture (Fig. 3, [25–28]). This yield increase was often thought to occur only in low input, subsistence farming systems because poor soils are made more fertile by the presence of a nitrogen-fixing legume crop [29]. Improved soil fertility would then boost the productivity of the other crop, often a grain. With the high rates of fertilization used in modern intensive agriculture, it was considered unlikely that soil fertility enhancement from intercropping would offer a competitive alternative to monocultures.
<figure><img src="image_5.png" /><figcaption>**Figure 3.** Magnitude of the increase in agricultural yields from intercropping (in %) compared to monocultures of the same two crop species. Values are derived from average (± standard error) Land Equivalent Ratios (LER) values calculated in four meta-analyses of the existing literature on intercropping. LER corresponds to the amount of land needed under monoculture to produce the same yield reached under intercropping. For instance, Martin-Guay et al. [28] found that one hectare under intercropping produces on average as much as 1.30 ha (LER) under monoculture. In other words, intercropping produces 30% more than a monoculture. Himmelstein et al. [27] did not provide standard error values for LER. Li et al. [25] provided two LER values, the higher corresponding to intercropping systems in which maize was one of the two crop species, and the lower which did not include maize. The number of data records, *n*, used in each meta-analysis.</figcaption></figure>

A meta-analysis of over 200 agricultural field experiments challenged this assumption by showing that an intensive version of intercropping, often called strip intercropping, can lead to surprisingly great yield increases for appropriate pairs of crop species [25,30]. In this modern version of intercropping, the usual high rates of fertilization of intensive agriculture are used. Each crop is grown in a narrow strip of land of about 1-2 m wide that contains several rows of the same crop species. The adjacent strip has several rows of the other crop, and strips of the two crops alternate. The yields achieved by this intensive form of strip intercropping were on average 29% greater than from monocultures of the same crops, and did so while using 36% less nitrogen fertilizer [25]. These benefits occur mainly because of seasonal differences in the growth, maturation and the height of the two crops grown [25,26,30]. Consider a cool-season crop, such as wheat or some legumes (like pea or soybean), grown with maize or another crop that grows best during the heat of summer and early autumn. Because the early season crop has stopped growing and been harvested by the time that the late-season crop is reaching its highest growth rate, there is minimal competition between the two crops. In this
178 "relay design" each crop can exploit, during its growth period, greater amounts of soil
179 nutrients, water and light than it could in a monoculture, thus giving a greater total harvest
180 than could either monoculture by itself.

181 To appreciate the difficulty of increasing yields 20% without intercropping, consider that the
182 current year-to-year yield increases for major crops average 1% or less per year. Thus, about
183 20 years of crop breeding and improvements in agricultural practices would be needed to
184 obtain the same yields in monocultures as intercropping could immediately achieve. Put
185 differently, 20% less land would have to be cleared if modern intensive intercropping were
186 adopted.

187 Beyond greater yields, there is much more that agriculture could gain by better exploiting
188 ecological complementarity differences between or within crops. Consistently across studies,
189 the yield benefits from intercropping occur even when 19% to 33% less fertilizer is used [25],
190 which thus decreases the pollution that occurs when unused nitrogen and phosphorous enters
191 groundwater, streams, rivers, lakes and oceans. Intermingling species and varieties also can
192 improve natural control of insects, diseases or weeds [28,31,32]. A multi-year experiment in
193 China found that strip intercropping of two rice varieties yielded 89% more than
194 monocultures, mainly because this controlled of a fungal disease that attacked one of the rice
195 varieties [33]. This natural control of disease was so effective that fungicide application was
196 no longer necessary after a few years, alleviating further harm to human health and to
197 biodiversity. Intercropping and variety mixtures can also help stabilize yields [34], increase
198 farmers' incomes [27] and can promote human health from increased dietary diversity [21].
199

200 **3. Breeding for biodiversity-based agricultural practices**

201 Traditional crop breeding has sought plant characteristics (i.e traits) that maximize yield in
202 monoculture. This approach can lead to low genetic variability within a crop genome and
203 individuals that are progressively more alike. However, such crops can be more susceptible to
204 variable weather conditions and to pests and diseases that spread rapidly over homogeneous
205 stands. Breeders know how to use long-standing genetic principles like hybrid vigor, to
206 reverse the tide of homogeneity and reintroduce genetic diversity within individuals. Indeed,
207 crossing parent plants with as much different gene sets as possible can produce hybrid
208 progeny that grow faster, produce more seed and fruits, and better resist stresses than either of
209 the parents [35].

210 Similarly, breeding efforts should address intercropping. Special varieties of a pair of crops
211 could be developed to maximize yields when grown together via intercropping, or similarly of
212 a single crop that would be grown as a mixture of varieties [36]. Thus far, breeding crops in
213 isolation from other genotypes or species and interactions among them deprived crops from
214 the forces promoting species coexistence in nature. In natural communities, each organism
215 develops a unique set of trait combinations, and like human professions, exploits different
216 aspects of the environment. Because these very differences among species underlie yield
217 gains and pest control [37], past human selection for monoculture performance may have
218 reduced the capacity of crops to perform better when co-occurring with other species.

219 This possibility was tested in a recent small-scale experiment that compared the gain in plant
220 biomass from crops (including tomatoes, millet, oats, wheat, peas etc) or their wild relatives
221 as the number of species in pots was increased [38]. As expected, biomass production was
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greater in mixtures of crops and wild relatives compared to monocultures. However, the magnitude of this diversity effect was 12% higher in mixtures of wild plants. This difference was attributed to the greater leaf area of crop wild relatives, a competitive trait.

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These results and others [39] suggest that breeding for uniformity within a crop may miss yield advances that might be obtained by breeding for greater genetic variation, or by planting genotypic mixtures of same crop species that exploit trait variability to minimize disease incidence and intraspecific competition, or that select for differences in competitive abilities.

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## Conclusions

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A fuller use of all levels of biodiversity in agriculture, deployed on spatial scales ranging from within-field to national levels, seems to have the potential to increase agricultural productivity and its year-to-year reliability while decreasing its environmental impacts and supporting nutritious diets. We have focused on three ways to increase biodiversity, but there are also other possibilities. One well-known approach is to increase crop diversity by alternating crops through time in rotations. Other possible means of diversification include cover crops, pest trap crops, and pest repellent crops, and diversifying agricultural landscapes, all of which merit exploration to determine if they benefit agriculture, the environment and society [40].

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Given the potentially large contributions that biodiversity-based practices could make for agricultural sustainability, it is surprising that they are only seldom used by farmers or encouraged by policy makers in most countries. Just as wind power and solar power required governmental aid before becoming profitable on their own, a shift toward global adoption of intercropping and other diversifying agricultural practices will require investments in research. This research should seek to find the best combinations of crop species and varieties as well as the spatial and temporal patterns for each region, and to underwrite the cost of developing the new agricultural machinery required, for instance, to plant, cultivate and harvest adjacent strips of different crops. Pending more efforts to mainstream diversified cropping systems, accelerating global demand for food will continue to be met by increased cropland areas, increased agricultural greenhouse gas emissions, and increased environmental pollution from agricultural fertilizer and pesticides. The biodiversification of agriculture has the potential to provide numerous environmental and health benefits.

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## Acknowledgements

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Research leading to this contribution was supported by the French National Research Agency (ANR) under the 'Programme d'Investissements d'Avenir' (reference 17-MPGA-0004).

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