Although the concept of mimicry is not dependant on a specific kind of ecosystem, some ecosystems were more often used for testing the mimicry hypotheses. Main natural systems used as models for agriculture include the rainforest ecosystem, the dry tropical forest model and the American prairie. We examine in the following how these three ecosystems serve as models and then how concepts defined for natural systems can be applicable to agricultural systems.
Natural system models at the basis of mimicry
The rainforest model
One of the main natural models underlying the mimicry theory is the rainforest model proposed by Ewel (1986) for the humid Tropics. According to Ewel (1999), humid tropical ecosystems appear to be particularly suitable for application of the “mimicry of Nature” concept. The tropical rainforest that combine multiple strata, incorporate a high specific diversity constitute a model for agroforestry systems. Agroforestry systems combine annual and perennial, herbaceous and woody species, in a complex system in terms of the number of plant species, biological interactions, and practices (Torquebiau 2007). Widespread in Asia, Oceania, Africa, and Latin America, they ensure both subsistence for local populations and major environmental and socio-economic services (Sanchez 1995; Nair 2001; Schroth et al. 2001, 2004; Figs. 3, 4, and 5). These agroforests contain many useful species and reach states and structures close to those of the original natural forest ecosystems. Yet the latter take more than half a century to develop, after gradual management involving several successive phases. It is by gradually reconstructing a suitable environment adapted to the biology of the different plants that it has been possible to exploit the different useful species. Regarding biodiversity, agroforests reach levels that can be compared in some cases to those found in nearby natural forests (comparison of the number of species present out of the major biological groups: trees, shrubs, creepers, herbaceous plants, epiphytes). The same applies to animal biodiversity (Perfecto et al. 1996; Leakey 1999; Perfecto and Armbrecht 2003).
Such properties can be found in the humid tropical zones of Asia, Africa, and Latin America, thereby affording generic properties to complex agroforestry systems. Some functions, such as maintaining biological diversity, maintaining biomass storage potential, and maintaining potential for the regulation of major biogeochemical fluxes, play an overall ecological regulator role. These agroforestry systems stand out from specialised cropping systems through three essential aspects arising from natural ecosystems: (1) their functioning is based on relations between species (competition, facilitation), (2) they offer high constituent biodiversity, and (3) they produce a multiplicity of products and environmental services that monocultures do not offer.
The dry forest model
Mimicry principles can be applied not only to the humid tropics but also to other agroecological areas such as the sub-humid and semi-arid tropics. Van Noordwijk and Ong (1999) considered the savannah zone where ecosystems are characterised by strong seasonality related to water stress and where natural vegetation is a continuous vegetation dominated by C4 grasses and scattered trees and shrubs. Agrosystems in that zone include agroforestry systems where food crops replace understorey grass and where many of the mature original trees are kept, thereby maintaining overall natural ecosystem functioning. The authors reported that attempts to improve the productivity of this system with fast-growing leguminous trees often failed due to greater competition for water with food crops. The traditional system often includes fallow–crop rotations, where the density of shrubs and tree biomass increases during the fallow phase and is maintained at a low level during the crop phase. Above-ground tree density in these parklands may be low but tree roots are in fact shown to exploit all the land area through large root extension.
Another example of savannah-like agroecosystems is given by Joffre et al. (1999) in the Mediterranean climate of the southwestern Iberian Peninsula. The dehesa system is a typical savannah-like agroforestry system characterised by an open tree layer, mainly dominated by Mediterranean evergreen oaks, and an herbaceous layercomposed of either cultivated cereals such as oats or wheat, or more commonly native annual species used as grazing resources. In this several millennia-old system, trees are planted, pruned, and harvested and are an integrated part of the system. The stability of this dehesa system has been shown to be highly dependent on water resources, nutrient availability, and human management in a long-term perspective. Tree density, a major indicator of the structure of the ecosystem and the result of long-term management by farmers, is greatly linked to mean annual rainfall, corresponding to an optimum functional equilibrium based on the hydrological balance.
The prairie model
Natural grassland ecosystems may be another model for agriculture: based on plant biodiversity, they protect the soil, provide their own nitrogen requirements, and are resilient to pests and diseases. According to Piper (1999), agricultural systems designed as structural and functional analogues of prairie plant communities can be productive and resilient. It becomes possible to conceive polycultures of perennial grain plants whose species composition should include perennial C3 and C4 grasses, nitrogen-fixing species, and composites. Such perennial polycultures of grains, in mimicry of the American Prairie, will require new crop species, selected according to new criteria other than those used for intensive industrial agriculture.
These three mimicry models highlight the critical importance of biodiversity in the mimicry concept. Beyond the “models” represented by humid and dry forest ecosystems and by prairie ecosystems, it is now important to indicate the main hypotheses at the basis of the mimicry theory and identify the ecology concepts that can be used to design sustainable cropping systems.
Hypotheses and concepts
Biodiversity and the mimicry hypotheses
The role of biological diversity in natural ecosystem functioning has been and remains the subject of much work in the community of ecologists. A great deal of recent work has shown some positive correlations between biodiversity and primary productivity, nutrient retention and post-stress resilience in natural ecosystems (Hector et al. 1999; Loreau et al. 2001), but also in cultivated ecosystems (Altieri 1999). Since Darwin, the hypothesis that the stability and sustainability of ecosystems rely on their biological diversity has appeared in numerous studies (and debates) involving ecologists. Tilman et al. (1996) assessed the sustainability of numerous prairie ecosystems characterised by different levels of biological diversity (number of plant species present). The fact that sustainability indicators, such as the degree of mineral nutrient recycling but also productivity, increase in line with biological diversity confirms the general opinion, but especially opens up new interesting prospects for prairie management, as shown by Piper (1999). In reality, the general hypothesis that a complex community is more stable than a community consisting of a limited number of species largely remains to be confirmed and any such confirmation seems to depend on a large number of factors. Vitousek and Hooper (1993) showed that the relation between the number of species in an ecosystem and the functions ensured by that ecosystem, e.g. primary productivity, is usually of an asymptotic nature: a relatively small number of species is likely to reach a high level of efficiency for the function in question.
While the actual number or species is no guarantee of stability, most authors agree in acknowledging the importance of functional diversity (Silver et al. 1996; Hooper et al. 2005) in the stability and resilience of ecosystems. For Gunderson and Holling (2002), the very definition of resilience incorporates the notion of functional sustainability, e.g. maintaining the integrity of functions, much more than that of structural sustainability, e.g. maintaining the integrity of species.
Consideration of heterogeneity as a potential source of stability is more recent in ecology. The idea has been developing relatively recently with the development of landscape ecology (Wu and Loucks 1995). It is thus possible to consider heterogeneous ecosystems, formed by patchworks of ecosystems subjected to recurrent disturbances like fire, as stable.
Ecosystems with greater diversity are more likely to contain multiple interactions and feedback loops associated with more complex food webs: this may be of great interest for agroecosystem resilience. Some authors call for the conservation of all the species in the system, as the elimination of species may compromise the integrity of the system. Beyond the fact that it is certainly unrealistic to conserve all species in a mimicry approach, this should focus our attention on the need to identify redundant species for identified functional groups, so as to conserve the function through identified species.
Another argument for maximising biodiversity in ecosystems is that ecosystems with greater diversity are more likely to contain the most productive species. This is probably true for natural ecosystems but it is of little interest for agroecosystems, as productive species are chosen by farmers.
Positive correlations between biodiversity and productivity, nutrient retention, and post-stress resilience have also been found in cultivated ecosystems (Altieri 1999; Malézieux et al. 2009). What biological diversity should therefore be chosen to optimise these different factors within cropping systems? Ewel (1999) and Van Noordwijk and Ong (1999) proposed two mimicry hypotheses for designing agrosystems from natural ecosystems:
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The first hypothesis argues that agrosystems should mimic the structure and function of natural ecosystems existing in a given pedoclimatic zone. It is based on the principle that the structure of natural ecosystems in a given area results from natural selection and therefore has a major ability to adapt and adjust to disturbances. Arguing that natural selection mainly acts on the level of genes, individual and family groups, Denison et al. (2003) criticised the validity of the first hypothesis and considered there is no reason to expect the structure of natural ecosystems to be a relevant source of inspiration for improving agriculture. This is, of course, an important and fundamental point of controversy.
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The second hypothesis argues that agrosystems should mimic the diversity of species existing in natural ecosystems too, hence maintaining the diversity existing in the natural ecosystems in a given zone. In the long debate on the relationship between agriculture and biodiversity, and more precisely in the debate on segregation vs. integration strategies for conservation, the second mimicry hypothesis clearly benefits the integration strategy that consists in maximising diversity in agricultural systems.
In their attempt to define ecological engineering, Bergen et al. (2001) identified five main principles. Most of these principles might be considered of great interest for cropping system design, although they were not defined for that purpose. The first principle promotes a design based on the “mimicry of natural structures and processes”. It emphasises self-organisation in ecosystems based on complexity and diversity. The second principle is based on the site-specific aspect as opposed to standardised solutions. Both principles may be considered at the basis of the “mimicry theory” in agriculture.
Productivity, resilience, equilibrium, and stability
The concepts of production, efficiency, stability and resilience, as defined by Holling (1973), lie at the heart of natural ecosystem characterization by ecologists. They were proposed by Fresco and Kroonenberg (1992) to assess agrosystems, but in reality their use remains very limited.
The production (or productivity) concept is a concept familiar to agronomists, although it is often used to consider useful yield, whereas it is first and foremost the primary productivity of the ecosystem that ecologists are interested in. This difference in objective and time step for assessing ecosystems is very important since it involves the very principle of agriculture, which consists in increasing the “take-off” of materials of use to mankind. Can mimicry of natural ecosystems provide the yields expected from modern agriculture? Few studies provide answers to this question but Ewel (1999) suggested this will hardly be the case for two main reasons. Firstly, only a small share of biomass is harvested from natural ecosystems. Agroforestry systems are characterised by high carbon investment in structure but only a fraction can be exported. Secondly, most ecosystems are characterised by a trade-off between reproduction, e.g. carbon dedicated to seeds, and permanence, e.g. carbon dedicated to structure, that do not allow high seed harvests. As already noted by Ewel (1986), if the benefit of nature-like ecosystems is low risk, their limitation may be low yield. Annual crops often have higher net primary productivity than perennial crops, and much of that productivity is allocated to the reproductive or storage organs harvested for food. Conversely, the energy allocated to structure in perennials and the small amount of biomass harvested determines low yields but allow ecological functions to be maintained. Hence, perennial polycultures built on nature mimicry may be sustainable cropping systems for the future, but they still have biological constraints in term of productivity. Although this may remain true from a carbon balance point of view, the mimicry system can be efficient if we consider the nutritional, economic, and social value of the various products exported from complex mimicry agrosystems: addition of the masses of the various products extracted from mimicry agroforestry systems has a limited interest compared to the social benefits of medicine, spices, fruits, tubers, wood, etc. extracted from the agrosystem.
Resilience is a property of major interest for ecologists who are interested in natural ecosystems. The resilience concept is therefore widely used today in ecology, but sometimes with different senses. Resilience is defined as the ability of an ecosystem to reorganise itself and restore its initial structure and functioning after a disturbance. This is a major ecological characteristic, which reflects the nature and complexity of the homeostatic processes in an ecosystem. Westman (1978) specifies that the resilience of an ecosystem can be characterised by its elasticity (time needed for restoration), its amplitude (degree of modification reached before restoration), its hysteresis (varying degree of asymmetry in alteration and restoration paths) and its malleability (capacity of the ecosystem to undergo frequent modifications). More recently, Walker et al. (2004) proposed other attributes for ecosystem resilience: latitude (deformation limit beyond which a return to the initial state is impossible), resistance (varying degree of a system’s ability to change), precarity (closeness of the current state of the system to a “point of no return”), and panarchy (dependency of the system in relation to hazards and factors outside the system). Other ecosystem attributes have also been defined, such as inertia which is the capacity of an ecosystem to resist a change in its structure and its function after a disturbance. Some are essential for analysing, in particular, the evolution of ecosystems inhabited by humans, such as adaptability and transformability (Walker et al. 2004). For instance, adaptability is defined as the ability of players in a system to influence resilience. Transformability corresponds to the ability to create a new system when ecological, economic, and social conditions have become unbearable. What are the sense and relevance of the attributes inertia, resilience, adaptability, and transformability when applied to cropping systems and to agricultural systems in general? Do these attributes enable a better characterization of this concept and the way it should be approached and used? How does the level of biodiversity affect resilience and inertia? These questions are increasingly vital within the agricultural research community. For example, one can thus consider that Sahelian cropping systems, which are based on the exclusive cultivation of millet (the only plant adapted to the ecological environment), have low resilience (low amplitude in relation to the absence of choice, great precarity, for example, in relation to a drop in rainfall), low adaptability, and low transformability (no alternative options). The duration of fallow needed to maintain yields in slash-and-burn cropping systems is another possible application: What is the possible amplitude of the system? What is its elasticity? An attempt can thus be made to generalise the use of these attributes for cropping systems. A cropping system can be in a situation of precarity (close to a state of no return), easy to modify (low resistance), highly dependent on the outside (panarchy), adaptable, transformable, or not very transformable. For example, intensive monocultures can be considered precarious and not very adaptable (insofar as, for example, parasite control is based exclusively on pesticide use), tree crop-based systems are less adaptable and less transformable than annual crop-based systems, etc.
Stability is another controversial attribute. The validity and operationality of many concepts in ecology are being discussed today within the actual community of ecologists itself (O’Neill 2001). The very definition of the “natural” vegetation of an ecosystem is the subject of debates, or even controversies in ecology (Sprugel 1991). It is considered today that most natural ecosystems cannot be considered in equilibrium: they are continually evolving in response to a changing environment (under the effect of more or less frequent disturbances, or climate change). In this context, the very concept of natural vegetation no longer has a sense, since we are faced with an ongoing and dynamic recomposition of the vegetation in terms of species. The hypothesis of the existence of a “climax”, an optimum state of equilibrium endowed with particular properties of homeostasis is now mostly challenged. If this climax concept is inoperative, it has to be considered that the structure of ecosystems evolves in response to natural disturbances of varying amplitude or frequency (fires, floods, climate changes, etc.). Whereas a frequent and regular disturbance will be a factor of stability for the vegetation, the absence of disturbance gives rise to changes in vegetation structure: other species follow on from the species adapted to the disturbance. Disturbance then becomes a factor of stability for the ecosystem. Thus, since the beginnings of agriculture, mankind has used fire to disturb the ecosystem, thereby mimicking nature. The advantages are numerous for a crop planted after burning: reduced competition for light, thermal destruction of weed seeds, provision of mineral nutrients.
Imposed organisation vs. self-organisation
One of the main concepts at the basis of ecological engineering is the self-designing capacity of ecosystems: self-organisation is the property of ecosystems to reorganize themselves given an environment that is inherently unstable and non-homogeneous (Mitsch and Jorgensen 2003). Self-organisation, a property of natural ecosystems, is generally opposite to the imposed organisation of agriculture. If self-organisation develops flexible networks with a high potential for adaptation, would it be possible to take inspiration from self-organisation in natural ecosystems to define an imposed organisation? The ecosystem “designs a mix of man-made and ecological components in a pattern that maximises performance, because it reinforces the strongest of alternative pathways that are provided by the variety of species and human initiatives” (Odum 1989).
Today, these notions seem essential for dealing with the long-term evolution of cropping systems, such as slash-and-burn agriculture where the cyclically recurring fallow may enable a return to an initial state, or complex agroforestry systems that combine several species over different time steps and in which the species may have varied functions. The evolution of a cropping system involves all the stands that compose it, i.e. all the biological objects composing the biocoenosis: cultivated and uncultivated plants, animal communities, soil microflora, etc. How are colonisation, competition, predation, mutualism, and extinction processes involved in that succession? How do human interventions, in their turn, act in these processes to control that evolution? It is possible, with natural ecosystems, to see autogenous successions that correspond to successions governed by internal processes (e.g. when there is a reduction in organic matter in the soil that leads to a change in the biocoenosis) and allogenous successions (when the successions are governed by outside processes), and such distinctions remain relevant when dealing with successions in cropping systems.