The Role of Crop, Livestock, and Farmed Aquatic Intraspecific Diversity in Maintaining Ecosystem Services

Abstract

Most of the attention given to intraspecific crop, livestock, and aquaculture diversity in agricultural production systems has been targeted at their roles in providing provisioning services, such as food and fibre or their cultural services, providing non-material benefits, such as places for recreation and inspiration. The additional role that intraspecific crop, livestock, and aquaculture diversity has in providing regulating and supporting ecosystem services for agricultural productivity and ecosystem resilience has been largely neglected. A literature review was carried out across sectors (crop, livestock, aquaculture), both on the counterfactual, i.e., the lack of intraspecific diversity in the production system and on the direct and indirect roles that intraspecific diversity plays in maintaining seven of the regulating and supporting ecosystem services: (i) regulating pest and diseases; (ii) maintaining and regulating water and soil quality; (iii) regulating and improving the flow of reproductive diversity; (iv) buffering excess or lack of water; (v) regulating soil erosion; (vi) nutrient cycling in water and soil; and (vii) supporting habitat maintenance. Benefits from the use of intraspecific diversity, diversity per se, and adaptive traits include a limited use of chemical inputs and unsustainable practices and their negative impact on livelihoods, ecosystem functioning, and productivity. All sectors (crop, livestock, and aquaculture) should be examined in the agricultural production system to understand the provision of the different ecosystem services by intraspecific diversity. Differences in structure, functioning, and temporal and spatial scales of these sectors should also be considered. Supporting and regulating ecosystem services often have relatively longer-term processes than food provisioning and rely not only on the current diversity but also on its presence over time. The presented regulating and supporting ecosystem services rely on the presence of the diversity from the farm to the landscape and to agroecological zone. Neglecting the additional role that intraspecific crop, livestock, and aquaculture diversity has in providing regulating and supporting ecosystem services is shown in this review to be detrimental to agricultural productivity and landscape resilience.

1. Introduction

A considerable amount of agricultural biodiversity continues to be maintained in the agroecosystems of small-scale farmers, pastoralists, and aquaculture systems in the form of traditional crop varieties, livestock breeds, and farmed-fish types [1,2,3,4,5,6,7,8]. These varieties, breeds and farmed types as well as their potential inner genetic variability are referred to as intraspecific agricultural diversity. This intraspecific diversity is an essential part of the livelihood strategies for small-scale farming populations [9,10,11,12]. These small-scale farmers and pastoralists are providing nearly 30 percent of our global food production [13,14,15].

Domestication and selection of modern crop varieties and livestock breeds have resulted in the following overall characteristics: widespread, highly specialized, and requiring high-external inputs. These varieties and breeds are for the most part more genetically uniform than their ancestors, ensuring a calibrated and high production under specific conditions and inputs. The history of crop and livestock domestication was initiated some 12,000 years ago (10,000 BC). Over the last 150 years, modern breeding with the use of scientific tools and for commercial purposes has produced major genetic changes for some major crops such as rice, wheat, maize, high-value fruit and vegetables, and oilseeds, leading to a great loss of genetic diversity [5,16,17,18]. Despite this early history, for the livestock sector, it was only about two centuries ago that the concept of breed, and with it a much stronger selection towards phenotypically homogenized breeds, was implemented. Only decades ago, heavy selection pressures were used to improve breeds productivity without enough consideration on the importance of preserving their overall genetic diversity [19]. Genetic improvement and domestication are much more limited for aquatic organisms with the exception of a few fish species [8,20]. The genetic diversity found in wild fish populations and the level of domestication of farmed fish remains much lower than that of livestock, leaving great potential for future domestication through genetic improvement and improved husbandry [8,21,22,23]. There is therefore a general concern over how to best conserve this intraspecific diversity.

To date, the majority of attention given to intraspecific crop, livestock, and aquaculture diversity in agricultural production systems has been targeted at their roles in providing provisioning services, such as food and fibre [24,25,26,27] and, to a lesser extent, to cultural services that provide non-material benefits, such as places for recreation and inspiration [3,25,28,29,30,31,32,33,34,35,36,37,38,39,40]. Moreover, most of these studies have focussed on the use of specific adaptive traits from traditional genetic resources for breeding programmes and for marketing crop, livestock, or aquatic resources [21,41,42,43,44]. Much less attention has been given to the potential role that this intraspecific diversity has in providing ecosystem services for regulation and maintenance [45] and increasing resilience across all three sectors: crop, livestock, and aquatic genetic resources. Moreover, the counterfactual is missing from these studies: the question of how the lack of intraspecific diversity can affect regulating and supporting services. It should nevertheless be noted that most of the publications explored in the literature review refer to a variety of terminologies and classifications.

We conducted a literature review on a selection of regulation and maintenance ecosystem services associated with intraspecific diversity in agriculture. The targeted services are (i) pest and disease control; (ii) water conditions and regulation of soil quality; (iii) lifecycle maintenance through the flow of reproductive materials; (iv) water flow and extreme-water-event regulation; (v) maintenance of soil and soil conditions; (vi) nutrient cycling in soil and water; and (vii) habitat maintenance and protection. The names of the ecosystem services have been chosen based on the names found in the literature review and a tentative harmonization with the Common International Classification of Ecosystem Services (CICES) [45,46]. In this review, we focussed on major crops, both annual and perennial (fruit trees), where significant intraspecific diversity has been documented. For livestock, we examine diversity among and within breeds, concentrating on major livestock species. For aquaculture, the review is a first exploration in an unexploited field, and articles were found for a limited number of target species or groups. The provision of or contribution to several of the ecosystem services, such as water flow and extreme-water-event regulation, maintenance of soil conditions, or nutrient cycling (in soil and water), depends on the very presence of animals in the agroecosystems. Local livestock breeds commonly display higher levels of adaptability to local conditions as they have often co-evolved within specific production systems, sometimes in harsh and extreme conditions, and with limited inputs [24,47,48]. For each studied ecosystem service, we examine both the effect of the lack and the presence, at various temporal and spatial scales, of intraspecific diversity.

2. Methodology and Literature Characteristics

Building on the work of Hajjar and colleagues [10], which focussed on intraspecific crop diversity, this paper looks at the potential for crop, livestock, and aquatic genetic diversity to enhance specific ecosystem functions through diversity per se and adapted traits [10,49]. Starting with the counterfactual, we examined all examples of the relation between low intraspecific diversity in the production system and the studied ecosystem services. This is followed by a review of evidence where intraspecific diversity for crop, livestock, and aquatic organisms has played a role in providing and maintaining the ecosystem services considered.

This review is based on 202 publications from 1960 to 2024 found through abstract searches on AGRIS, CABI, CORE, and AGRICOLA, as well as a search on Google Scholar, Scopus, ScienceDirect, and Web of Science research portals. Keywords used for the search included the names of the different ecosystem services targeted as well as the words variet*, breed, intraspecific, genetic diversity, and genetic variability, filtered for the three sectors, crop, livestock, and aquaculture. It is important to note that when searching and filtering using the above keywords, publications that mention the characteristics of breeds, varieties, or farming types that enable them to thrive in particular environments, but without mentioning ecosystem services, were not selected. Publications from FAO and various development projects were also searched. From the very large number of publications obtained via the keyword search, a sub-selection was made by checking their titles, then abstracts, and then finally the full publications themselves. Thirty-eight of the publications searched helped develop the counterfactual. When examining the role of intraspecific genetic resources, 60% of the references clearly mentioned the intraspecific level while we had to search for additional publications demonstrating the presence of the intraspecific diversity in the given contexts for the remaining 40%.

In addition to the 202 publications, 69 references helped structure this paper and define the concepts.

Table 1. Number of publications on the role of each sector per studied ecosystem service.

	Definition	Crop	Livestock	Aquaculture
Pest and disease control	6	22	30	10
Water conditions and regulation of soil quality	5	12	13	19
Lifecycle maintenance through the flow of reproductive material	2	15	4	0
Water flow and extreme-water-event regulation	3	23	10	0
Maintenance of soil and soil conditions	3	7	12	0
Nutrient cycling in soil and water	3	11	9	13
Habitat maintenance and protection	15	11	15	20

presents the number of publications per sector and ecosystem service.

Slightly more than half of the publications gathered were not attached to a specific geographical location but either treated ecosystem services and functions in a general or worldwide manner or were based on experiments with controlled environments.

Table 2. Distribution of articles per World Region or in the category “general, experiment, global”.

World Region or General/Experiment/Global	Number of Publications
General/Experiment/Global	102
Africa	23
Europe	34
Asia	16
North America	8
Latin America and the Caribbeans	13
Oceania	3

summarizes these results with publications referring to specific World Regions or general regions experiments in controlled environments, or the global level. Note that some publications are reported in more than one World Region.

Journal articles represent 80% of the publications of this review. Other publications searched are books, book sections, technical papers, proceedings, and project and thesis reports.

Looking at the temporal distribution of the publications by sector and of publications explicitly mentioning the intraspecific level, presented in Figure 1, we see that the focus for publications on ecosystem services was first directed to the crop sector then slightly later to the livestock sector and then even more recently to the aquaculture sector.

3. Intraspecific Genetic Resources of Crops, Livestock, and Aquaculture and Their Role in Supporting and Regulating Ecosystems

Table 3. Intraspecific genetic resources of crop, livestock, and aquaculture and their role in supporting and regulating ecosystem services.

Ecosystem service and definition/sector/counterfactual (CF) and role (R) The first definitions and characterization of the target ecosystem services were found in the millennium ecosystem assessment [25]
Pest and disease control regulating pests and diseases includes reduction in crop damage by herbivory (e.g., insects) and pathogens and reduction in the risk of diseases and parasites to animals and farmed aquatic resources [27,50,51,52].
Crop CF Genetic uniformity of crops is linked to higher risks of epidemics [53,54,55] R The use of intraspecific crop diversity in the form of variety multilines, mixtures, and genetically variable populations is an efficient ecological approach for pest and disease control. Examples are found for apple trees, bananas and plantains, common beans, potatoes, rice, and wheat in various production systems [5,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70,71,72,73].
Livestock CF It has been shown that homogeneous populations do not suffer more epidemics, on average, but have more risks of catastrophic epidemics [74,75] R Different mathematical models indicate that high species diversity and intraspecific diversity limits the occurrence and strength of outbreaks. Many mammalian and avian indigenous breeds around the world show specific traits of tolerance or resistance to infectious and parasitic diseases and have high inner-breed genetic variability. More genetically diverse breeds will adapt better to changing contexts. The selection of specific resistance and tolerance traits for improved breeds is an important strategy in disease management. In the case of sheep and goats, specific breeds have shown tolerance to gastrointestinal worms, liver fluke, scrapie, and foot rot. Indigenous chickens, because of natural selection, under scavenging conditions, have inherited robustness and resistance to various diseases and have better survival rates than commercial breeds under village production conditions. Although a limited number of breeds are found in a single pasture, at larger levels, the diversity of landscapes and conditions requires adapted breeds for each of them [24,40,43,75,76,77,78,79,80,81,82,83,84,85,86,87,88,89,90,91,92,93,94,95,96,97,98,99,100].
Aquaculture CF Low intraspecific diversity for fish, algae, and molluscs is associated with higher virulence of and greater vulnerability to diseases and parasites [87,101,102,103,104]. R Several publications highlight the role of genetic diversity in the regulation of parasites and diseases in cultured and non-cultured aquatic organisms. The genetic diversity of host populations slows the adaptation of parasites [102,105,106,107,108,109].
Water conditions and regulation of soil quality Water and soil quality, in a context of ecosystem service, are defined by the level of pollution and its impact on human, animal, and natural ecosystems’ health. Water quality is determined by the composition of runoff coming from, inter alia, agriculture. Moreover, soil quality depends on soil capacity to function [110,111,112,113,114].
Crop CF Modern farming systems often imply high-external inputs (pesticides, fertilizers, antibiotics, hormones, water…) and low genetic diversity. Homogeneity in farmed crop varieties, livestock breeds and fish strains requires the use of these external inputs to support and maintain productivity [115]. R Cultivation of diverse local varieties or cultivars adapted to soil conditions and quality allows a limited use of chemical inputs and reduces the vulnerability of agroecosystems to biotic and abiotic stresses. Less need for chemical inputs in agriculture will preserve and improve soil quality. The role of the intraspecific diversity in this case is found at a larger level than on the field; rather, at agroecosystem level, a diversity of variety is requested for each specific condition. Intraspecific diversity via limiting the occurrence of pests and diseases reduces infestations and diseases and therefore the use of pesticides and the resulting pollution. For soil rehabilitation and the production on degraded soils, examples exist where intraspecific diversity is key [10,116,117,118,119,120,121,122,123,124,125].
Livestock CF No reference found for the counterfactual except the lack of adaptedness in harsh environments preventing the very presence of animals. R Overgrazing accelerates soil erosion; however, adapted rangeland management and grazing practices can support soil maintenance, controlling weed development and preventing fire and erosion. Breed effects on grazing behaviours have been observed for sheep and cattle. At the pasture level, there might be only one breed; however, in harsh conditions, breeds found are commonly indigenous ones that adapt to their environments due to their inner genetic variability. For improved breeds, the importance of the diversity is seen at larger scales but remains crucial [40,88,126,127,128,129,130,131,132,133,134,135,136]
Aquaculture CF Low intraspecific diversity is associated with lower fitness and lower health and higher inbreeding risks as well as susceptibility to environmental changes and therefore prevents the provision of the service [101,102,103,104,137] R The role of bivalves such as mussels and oysters in water filtration and nutrient removal and recycling is largely recognized. Results were found at species level; however, a positive relationship between genetic diversity and growth rate was found in shellfish, and higher growth rates result in higher rates of water filtration [102,138,139,140,141,142,143,144,145,146,147,148,149,150]. Moreover, farmed animals, plants, and algae with higher genetic diversity require less use of antibiotics and other chemicals, therefore leading to a better water quality (see pest and disease control).
Lifecycle maintenance through the flow of reproductive material Pollination is mediated by wind, water, or animals, mostly insects. In the context of ecosystem services, pollination generally refers to animal-assisted pollination [151]. Seed dispersal is the dispersal of the reproductive unit of a plant and is key in the long-term dynamics of plant communities [152,153]. Because of their roles in supporting biodiversity, regulating ecosystem processes, and providing natural resources, pollination and seed dispersal are considered an ecosystem service that contributes to human wellbeing [154,155].
Crop CF Agricultural intensification, featuring crop uniformity, causes habitat fragmentation and degradation, meaning reduction and even disappearance of food and nesting sites for pollinators [156,157,158,159,160,161]. R Pollinator-attracting genotypes and the planting of various varieties of certain crops enhance pollination services and the quality of fruit production. In fruit trees, the self-incompatibility of some cultivars requires the use of different varieties in one plantation to allow cross-pollination. Different varieties of the same crop with different flowering times can also be planted to increase the chances of pollinator population survival to the next growing season and the types of pollinators visiting at different times during the season [158,159,162,163,164,165,166,167,168].
Livestock CF No reference found for the counterfactual except the lack of adaptedness in harsh environments preventing the very presence of animals R Dispersal of seeds commonly happens through animal dung and coats, and sometimes hooves. Seed dispersal will vary depending on the fleece or fur, its structure, density and curliness or on the size and shape of hooves. Differences are noted at species level but also at breed level for some specific feeding behaviour and adaptation to specific environments [169,170,171,172].
Water flow and extreme-water-event regulation Extreme events may result in phenomena such as flooding and waterlogging with excess water and, drought, and water scarcity. Water scarcity can be defined as the reduced relative and absolute availability of the water resource. Water resource quality degradation is also considered as water scarcity but has been addressed in a previous section [173,174,175].
Crop CF Intensive irrigation practices are often associated with uniform crop populations that require high agricultural inputs to be productive [176]. R A permanent organic covering of the agricultural land and soil is reported to provide many benefits including soil structure and internal drainage that in turn impact soil water retention and water quantity regulation as observed in conservation agriculture and agroforestry. Varietal diversity allows improved spatial and temporal cover by providing the genetic diversity for short- and long-cycle varieties, for winter varieties, and for specific environments and soils. In situations of excess water, diversity offers options of varieties adapted to specific conditions such as excess of water. In situations where water is lacking, varietal diversity, with different responses to hydric stress and tolerance to drought, enables farmers to have a harvest in drought-prone areas. Examples are found for date palm, durum wheat, faba beans, maize, pearl millet and sorghum, okra. Adapted varieties also require lower levels of irrigation, thus sparing water for other uses [10,39,125,177,178,179,180,181,182,183,184,185,186,187,188,189,190,191,192,193,194,195].
Livestock CF Exotic breeds that have been selected for their high production potential are very homogenous genetically and require high input conditions, including water. High levels of water consumption, especially in contexts of drought and water scarcity increase the overuse of water and have effects strictly opposite to buffering [24,196,197,198]. R Indigenous and locally adapted breeds of various livestock species, particularly goats, show a good adaptation to drought conditions and heat stress. These breeds also present a high within breed genetic variability. Overall high-yield improved breeds tend to be more susceptible to heat stress. In situations where water is lacking, adapted breeds, because of their ability to survive and produce in these conditions, will consume and use lower quantities of water, thus allowing this water to be available for other purposes [24,43,95,196,199,200,201,202,203].
Maintenance of soil and soil conditions Soil erosion occurs when the removal of topsoil by water, tillage, or wind is faster than the soil forming processes replacing it; this can be due to natural, animal, or human activity. Regulating soil erosion is guaranteeing a constant soil cover and preventing soil issues from exposition to erosion [204,205,206,207].
Crop CF Large-scaled, highly mechanized, and monoculture-based systems, characteristics of intensive farming, often result in poor soil protection, leading to erosion [208,209]. R In agroecosystems, besides the use of conservation agriculture, the soil is left bare after one cropping cycle and is exposed to erosion. Environmental factors influence crop survival based on their traits and characteristics. When crops survive, they help to reduce erosion, because their presence all along the season ensures that the soil is covered with a continuously present biomass. This is the case for varieties of cowpea, maize, millet, rice, and sorghum. Intraspecific crop genetic diversity allows for an enhanced and extended soil cover, thus preventing soil erosion [116,190,210,211,212].
Livestock CF No reference found for this counterfactual except the lack of adaptedness in harsh environments preventing the very presence of animals R Grazing management allows controlling the amount of remaining plant, limiting risks of fire and erosion. Grazing characteristics and efficiency will depend on species, breeds, and individuals. Differences in grazing behaviour will vary with animal body size, preferences for forages, age, and physiological status of the animals and plant palatability. Stocking rates should be adapted to the species and breeds depending on their grazing behaviour and performance and on the carrying capacity of the pasture. Indigenous breeds present a high within breed genetic variability, allowing them to be present in harsh conditions. For other breeds, the importance of diversity is seen at larger scales [40,126,127,128,129,130,131,132,133,135,136,201].
Nutrient cycling in soil and water The nutrient cycle is a concept that describes the flows of nutrients between physical environments and living organisms. Examples include the carbon nitrogen and the phosphorus cycles [213,214,215].
Crop CF Studies have demonstrated that monocultures alter soil health, including nutrient cycling. Continuous monoculture in the same field negatively impacts the functional microbial diversity of the soil and causes the accumulation of certain host-specific pathogens. It also leads to an imbalance in the nutrient content of the soil [216,217,218,219]. R Research on intentional introduction of soil micro-organisms to increase soil biodiversity and aid in nutrient dynamics has shown that cultivars of various crops do not respond similarly, physiologically, or morphologically, to inoculation with mycorrhizae. Studies have been conducted for fava beans, pearl millet, wheat, and olive trees. Soil respiration increases with intraspecific leaf litter diversity [220,221,222,223,224,225,226].
Livestock CF No reference found for the counterfactual except the lack of adaptedness in harsh environments preventing the very presence of animals. R Grazing transfers nutrients from the pasture to the grazing animals, enabling them to grow. Some nutrients are returned to the soil through dung and urine. Different breeds present different grazing behaviour, aptitude for fibre digestibility, or capacity to “walk” a lot; this is particularly relevant for cattle breeds, and they adapt to their harsh environments. Local breeds are well adapted to thrive on food waste and crop residues and by-products. Indigenous breeds usually present a high within breed genetic variability, allowing them to be present in harsh conditions. For other breeds, the importance of the diversity is seen at larger scales [47,227,228,229,230,231,232,233,234].
Aquaculture CF Low intraspecific diversity is associated with lower fitness and lower health and higher inbreeding risks as well as susceptibility to environmental changes and therefore prevents the provision of the service [101,102,103,104,137]. R Farmed seaweeds and shellfish participates in nutrient cycling and nutrient removal when harvested. Results were found at species level; however, fitness and health of farmed populations depend, inter alia, on their intraspecific diversity [87,142,144,146,148,235,236,237,238].
Habitat maintenance and protection A habitat is an area occupied and supporting living organisms. It is also used to mean the environmental attributes required by a particular species or its ecological niche. A habitat is made up of physical factors such as soil, moisture, range of temperature, and availability of light, as well as biotic factors such as the availability of food and the presence of predators [151,239,240].
Crop CF Habitat fragmentation and loss is commonly reported under agricultural systems with low intraspecific diversity. The larger the scale of the monoculture, the higher the impact on native species [241,242,243,244,245,246,247,248]. R In intrinsically diverse and variable production systems, crop genetic diversity, with the diversity of traits and interactions it provides, allows niche complementarity, a better use of the resources available, including nutrients, and enhances productivity and biomass production. They are not polluted by agrochemicals and prove to be stable and resilient habitats. These types of diverse production systems tend, however, to be on small surfaces [10,116,210].
Livestock CF No reference was found for this counterfactual except the lack of adaptedness in harsh environments preventing the very presence of animals. R Adapted low intensity grazing by livestock creates or maintains specific habitats for wild plants and animals, and these seminatural environments are identified as crucial for habitat maintenance. Habitats with high value or high diversity are often located in areas with particular or extreme conditions (mountainous, dryland, marginal, or forest areas) and are mostly grazed by locally adapted breeds. Different livestock species and breeds have different grazing and foraging behaviours and diet, and goats are recognized as important for preventing woody encroachment and fire risks. Indigenous breeds usually present a high within breed genetic variability, allowing them to be present in harsh conditions. For other breeds, the importance of diversity is seen at larger scales [24,40,170,249,250,251,252,253,254,255,256,257,258,259,260].
Aquaculture CF Low intraspecific diversity is associated with lower fitness and lower health and higher inbreeding risks as well as susceptibility to environmental changes and therefore prevents the provision of the service [101,102,103,104,137]. R Shellfish and seaweed aquaculture is largely recognized for their provision of habitat to a large diversity of aquatic organisms. Results were found at species level; however, fitness and health of farmed populations depend, inter alia, on their intraspecific diversity [109,137,143,238,261,262,263,264,265,266,267,268,269,270,271].

presents the results of the literature review for the three sectors for each targeted ecosystem service. Counterfactual elements are also reported.

Based on the literature review conducted, we identified the main negative impacts of low intraspecific agricultural diversity and the potential roles of its presence in the production system. Positive effects of low diversity, such as the simplification of the work, are not reported and were not studied.

Table 4. Effects in the production system of low intraspecific agricultural diversity and of its presence for the studied ecosystem services for regulation and maintenance.

Impact of Low Diversity	Ecosystem Service	Role of Intraspecific Diversity
Occurrence and outcome of epidemics	Pest and disease control	Means to reduce pest and disease epidemics and outcome
Pesticide and antibiotic overuse; Nutrients and hormones toxicity	Water conditions and regulation of soil quality	Substitute for agrochemicals
Habitat fragmentation and degradation	Lifecycle maintenance through the flow of reproductive material	Means for habitat creation and renewal
Extreme water events (flooding/drought)	Water flow and water extreme events regulation	Means for improved water management
Soil erosion	Maintenance of soil conditions	Means for soil maintenance and rehabilitation
Nutrient loss	Nutrient cycling in soil and water	Means for improved nutrient cycle management
Habitat fragmentation and degradation	Habitat maintenance and protection	Means for habitat creation and renewal

presents these results.

From the literature review, we find that, when documented, low intraspecific diversity has a direct negative impact on ecosystem services, particularly when replaced with chemical agricultural inputs and unsustainable management practices. In turn, these chemical inputs and management practices have indirect negative effects on several ecosystem services such as pest and disease regulation or soil and water quality regulation. Moreover, because of the many interlinks between regulating and supporting ecosystem services, low diversity often has a negative domino effect.

Low intraspecific diversity affects the regulation of pest and disease in the agroecosystem: not only is the service lost or limited, but there is an increased use of agrochemicals; this in turn leads to the indirect effect of increased disease and pest resistance to chemicals, as well as a larger spread of epidemics and infestations because of genetic uniformity. For water and soil quality regulation, direct effects are similar with loss of service, but indirect effects take the form of soil and water pollution, the use of agrochemicals, and other unsustainable agriculture practices. Direct effects are similar for nutrient cycling with indirect effects being the disruption of nutrient cycles and their replacement by human interventions. In the case of pollination and seed dispersal, the direct effect of low intraspecific diversity is the loss of natural populations providing the ecosystem service and therefore of the service itself and the introduction of beehives or manual pollination practices as a replacement. Indirect effects are found in another type of ecosystem service: food provision. For buffering excess and lack of water, low diversity has mainly indirect impact with the degradation of the service in the form of more extreme water events or the establishment of water retention infrastructures such as dams and reservoirs. Similarly for soil erosion regulation, the indirect effects of low diversity are the degradation of the service with soil erosion and the increased use of heavy tillage and other non-conservation agriculture practices. Finally, the impact of low diversity on habitat maintenance is the cumulation of direct effects for the other regulating and supporting ecosystems services leading to poor habitat quality; indirect effects are habitat destruction or fragmentation because of poor soil management, extreme events, etc. This is coherent with the results gathered by Duval and colleagues [272] for the contribution of agrobiodiversity, from the ecosystem level to the intraspecific level, to the resilience of production systems.

This diversity also acts as an abatement factor for loss as an alternative to moderating or reducing the use of chemicals and medical treatments and, as such, has an impact on water and soil quality [119,273].

We also find that, while faunal ecosystem services—such as pollination, pest and disease control, and seed dispersal—are largely considered to be strictly provided by wildlife population, the potential of domesticated animals to contribute to these regulation services should be considered [50].

In aquaculture, genetic variability appears to be an asset sometimes resulting from an adaptation to environments [274]. Ecosystem-based approaches are key to the sustainable development of aquaculture with the inclusion of potentially regulating and supporting ecosystem services provided by these production systems [275].

Temporal and Spatial Scales

Spatial and temporal scales at which intraspecific diversity occurs and matters are closely linked to the characteristics of each sector and to the scales at which ecosystem services are produced.

The use of a single variety, breed, or farmed aquatic type as being deliberately chosen for adaptation to a specific environment is distinguished from the use of diversity per se as insurance to maintain regulating and supporting services under heterogeneous environments or changing environmental or social economic conditions. Adaptive traits in agricultural systems allow production for specific conditions at a given time. Diversity per se allows us to ensure productivity over time, have sustainable production, or have diversity to choose from in the future. Different farmers have different populations of the same crop variety [276]. Genetically diverse livestock populations provide the society with a greater range of options for meeting future challenges. They allow farmers and pastoralists to select stocks or develop new breeds in response to changing conditions, including climate change, new or resurgent disease threats, new knowledge of human nutritional requirements, and changing market conditions or changing societal needs. If they are lost, the options for future generations will be severely curtailed [24,277]. Many endangered breeds are found in harsh production systems and may possess unique genetic adaptations and disease-resistance characteristics [278]. Moreover, when focussing on adaptive traits, it is possible to have a limited number of breeds or varieties that have been selected for specific conditions, sometimes at a very small geographical scale in case of soil characteristics or uneven terrains used at small levels. Looking at larger spatial scales, landscape to agroecological zones, the diversity of all the selected breeds and varieties appears again as key for thriving in all the conditions included at these scales [279]. Another important element to note is that although overall genetic diversity might be high, functional diversity can be low if the various varieties and breeds all carry the same selected functional traits. A diversity of functional traits are important for farmers and livestock keepers to enable them to adapt to changing environmental and socio-economic conditions [5,280,281].

Based on the various publications collected during the literature review, Figure 2 presents a schematic view comparing the spatial and temporal “starting points” of crop, livestock, and aquaculture intraspecific diversity’s impact on provisioning and supporting ecosystem services. While the spatial aspects vary depending on the characteristics of the sector studied, the minimum temporal scales where diversity impacts these services are more closely linked to the operating timeframe of a given ecosystem service. Axes present the order of magnitude and do not pretend to propose precise values. Figure 2 is the result of the authors’ analysis of the many publications gathered.

For the spatial scale axis, we considered the farm or household level, the community and landscape or seascape, the agroecosystem level, and then wider with no reference. We refer to a local community as a social geographic group where people at a particular point in time have common interests and live in a defined geographical area, rural or urban, within a broader society [17]. For the temporal axis, we considered growing seasons, years, and decades as they are the timeframe for production and lifespan for the different sectors.

For pest and disease control, we found from the literature review that spatial scales where diversity matters are small, as for all sectors, intraspecific diversity at plot, pasture, or pond level means better tolerance or resistance to pests, diseases, and parasites. For livestock, the intraspecific diversity is found at small spatial scales in indigenous or locally adapted breeds kept by local communities. For these breeds, a wide array of traits and plasticity has been shown within and between breeds, indicating that livestock genetic diversity provides a range of options that are likely to be valuable in climate change adaptation, including tolerance of climatic extremes such as hot temperatures, adaptation to poor-quality diets or to feeding in harsh conditions, and resistance and tolerance to specific diseases [24]. Indigenous breeds thrive in harsh environments but generally do not have high productivity rates [282,283]. Temporal scales where intraspecific diversity is key for pest and disease control follow the temporal scales of the lifespan of the domesticated plants, animals, or aquatic organisms. Lifespan, reproductive maturity, and intervals between generations vary greatly for the different sectors and for species within a sector, from annual crops to perennial crops, from cattle to poultry, from bivalves to algae.

In the case of water conditions and regulation of soil quality, spatial scales are small for crops where multiple varieties can be adapted to a given plot and for aquaculture where healthy bivalves and algae are genetically diverse. Larger spatial scales are found for livestock where breeds are adapted to each specific condition where their controlled grazing contributes to the service. The diversity is “found” only when taking a step back. The relevant temporal scale is short for aquaculture with constant filtration and nutrient removal activities. It is also short for crops depending on growing seasons. The temporal scale depends on the lifespan of animals for livestock. For lifecycle maintenance through the flow of reproductive material, we found that for the crop sector, the plot scale and the growing season are relevant, and in the case of livestock, larger scales for dispersal and lifespan of animals are relevant. For the ecosystem service maintenance of soil and soil conditions, we found for the crop sector that the plot scale, where varieties will protect the soil, is the starting point and the temporal framework of annual and perennial crops. Larger spatial scales are relevant for livestock breeds with their grazing ability and, again, the lifespans of animals. In the case of nutrient cycling in soil and water, plot levels and growing seasons are essential for crops. Livestock breeds’ presence and adaptedness across landscapes is required, and the time scale follows the lifespan or production period. As for aquaculture, we have a small spatial scale and production period. Habitat maintenance and protection are dependent on all the other regulation services, and the smallest and shortest scales are key for this service.

Selection, in all sectors, to obtain higher productivity brings light on the trade-offs between provisioning ecosystem services and regulation services [51,284]. Indigenous or local varieties, breeds, or farmed types that thrive better than selected ones in many harsh and changing environments will not have high production rates [201,282,283]. Management of genetically diverse rather than uniform systems can require more decision choices, time, and adapted processing equipment, for farmers and livestock keepers in the short term. However, managing diversity has the potential to maximize both current and future productivity and reduce the potential to future loss due to unsustainable management practices [285].

Because farmers and pastoralists must deal with obstacles and risks all along the production or growing season and from one season to the other, the temporal scale at which diversity occurs and operates will determine the use they make of it in their strategy for risk management. The spatial and temporal scales at which regulating and supporting ecosystem services are operating require the presence over these scales of the various service providers among which intraspecific genetic diversity in each sector when this diversity is contributing to the provision or maintenance of these services. Annual and perennial crops, livestock, and aquatic intraspecific diversity present different characteristics that are reflected in the scales from which they are first detected or the “starting point” when they have an impact on the provision of regulating and supporting ecosystem services. If the impact is detected at a small spatial or temporal scale, this is the “starting point” where it will continue to have impact at larger spatial and temporal scales.

In the case of annual crops, the household level, as well as short temporal scales such as growing seasons, is often crucial. For perennial crops, the landscape level is more present and important temporal scales will be years and decades. Livestock breed diversity matters at landscape level and longer temporal scales because of its spatial distribution and the lifespans of animals. Less information was gathered for aquatic farmed diversity, and therefore, the scales identified are more difficult to analyse although we know there are high levels of functional diversity at small scales. Overall, the contribution to regulating pests and diseases starts at small spatial and short temporal scales, while supporting habitat maintenance starts at larger and longer scales. Other studied ecosystem services are spread between those two extremes.

The different levels of genetic diversity within farmed crop varieties, livestock breeds, and aquatic populations are related to the length of the different sectors’ history of domestication and the lifespan of the entity considered. This is directly related to levels of genetic diversity available in improved varieties, breeds, and aquatic farmed populations. This timeline has meant that modern breeding has caused much higher levels of genetic erosion in crops than in livestock than, in turn, in aquatic farmed populations. Plants are not mobile themselves but their genetic material is; breeds are usually less diverse at the farm level, but they are mobile and can move from pasture to pasture, sometimes over a wide distance as potentially in transhumant or nomadic systems. This is also reflected in Figure 2.

4. Conclusions

The detrimental effects of low intraspecific diversity in all sectors (crop, livestock, and aquaculture) on supporting and regulating ecosystem services, on agricultural productivity, and on the overall ecosystem health are visible in the counterfactual information provided. Intraspecific diversity provides both direct and indirect benefits to agricultural productivity and ecosystem health. Diversity allows avoiding resorting to large quantities of chemical inputs and to unsustainable agronomic or zootechnical practices. This, in turn, limits the negative impact of the use of these inputs and practices and their damaging side effects on livelihoods, ecosystem functioning, and in the long-term on productivity gains. Both the diversity, per se, within a species and a species’ adaptive traits are crucial to deliver these benefits today and in the future, particularly in the context of climate change. Reaping these benefits, however, requires access to diversity and knowledge, intellectual investment in planning and organisation, and appropriate agricultural tools and policies supporting the use of agricultural diversity.

Temporal and spatial scales differ for the provision of the different ecosystem services by intraspecific diversity. Provisional ecosystem services in the form of the production of food and non-food products tend to have relatively short time scales, while supporting and regulating ecosystem services often have longer-term processes. Supporting and regulating services rely not only on the availability of the current diversity, but also the continued presence of diversity over time. Temporal and spatial scales for the provision of ecosystem services also differ according to sector. At landscape level, genetic diversity is found both between and within crop varieties. In contrast, for a given livestock species, genetic diversity is more likely found within a breed or between a small number of breeds rather than a community of farmers or pastoralists keeping animals of numerous distinct breeds. Diversity measured by the number of varieties compared to the number of breeds is likely to be higher for crops than for livestock at the farm, community, and landscape scales. In contrast, the levels of functional genetic diversity, for some selected traits, can be similar for crops and livestock (such as disease tolerance traits).

Agricultural production systems should be seen as holistic, using a comprehensive lens that includes the role of intraspecific diversity of crop, livestock, and aquaculture species as an integral part of the regulating and provisioning services they provide. While this approach needs to be cross-sectoral and interdisciplinary, differences across sectors in structure, functionality, and temporal and spatial scales must be taken into account. Neglecting the additional role that intraspecific crop, livestock, and aquaculture diversity has in providing regulating and supporting ecosystem services is detrimental to agricultural productivity for sustainable agriculture with lower agricultural inputs and landscape resilience. In order to better understand and benefit from agricultural biodiversity, data should be collected more systematically, enabling any correlations to be identified between crop varieties, livestock breeds, aquatic farmed types, the management practices adopted by farmers, livestock keepers, and ecological parameters.