Review Article |
Corresponding author: Claudia Gutierrez-Arellano ( claudia.gutierrez_arellano@kcl.ac.uk ) Academic editor: James S. Pryke
© 2018 Claudia Gutierrez-Arellano, Mark Mulligan.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Gutierrez-Arellano C, Mulligan M (2018) A review of regulation ecosystem services and disservices from faunal populations and potential impacts of agriculturalisation on their provision, globally. Nature Conservation 30: 1-39. https://doi.org/10.3897/natureconservation.30.26989
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Land use and cover change (LUCC) is the main cause of natural ecosystem degradation and biodiversity loss and can cause a decrease in ecosystem service provision. Animal populations are providers of some key regulation services: pollination, pest and disease control and seed dispersal, the so-called faunal ecosystem services (FES). Here we aim to give an overview on the current and future status of regulation FES in response to change from original habitat to agricultural land globally. FES are much more tightly linked to wildlife populations and biodiversity than are most ecosystem services, whose determinants are largely climatic and related to vegetation structure. Degradation of ecosystems by land use change thus has much more potential to affect FES. In this scoping review, we summarise the main findings showing the importance of animal populations as FES providers and as a source of ecosystem disservices; underlying causes of agriculturalisation impacts on FES and the potential condition of FES under future LUCC in relation to the expected demand for FES globally. Overall, studies support a positive relationship between FES provision and animal species richness and abundance. Agriculturalisation has negative effects on FES providers due to landscape homogenisation, habitat fragmentation and loss, microclimatic changes and development of population imbalance, causing species and population losses of key fauna, reducing services whilst enhancing disservices. Since evidence suggests an increase in FES demand worldwide is required to support increased farming, it is imperative to improve the understanding of agriculturalisation on FES supply and distribution. Spatial conservation prioritisation must factor in faunal ecosystem functions as the most biodiversity-relevant of all ecosystem services and that which most closely links sites of service provision of conservation value with nearby sites of service use to provide ecosystem services of agricultural and economic value.
crop raiding, disease control, providers, invasive species, pest control, pollination, seed dispersal
Biodiversity is recognised as a key support for stable life on Earth (
Animals are key ecosystem services providers; therefore, we denominate faunal ecosystem services (FES) as those services that rely heavily on animal population. Fauna is a source of provisioning (e.g.
An imbalance of animal populations may be the cause of reduced FES production and/or the generation of faunal ecosystem disservices, such as the occurrence of crop pests (e.g.
Regulation FES occur mostly at the local scale (
In this scoping review, we aim to give an overview of the current and future situation of regulation FES in response to agriculturalisation globally. We summarise the most relevant evidence addressing the following topics: a) the relevance of animal populations as providers of regulation services; b) the role of species richness and of abundance of providers in regulation FES provision; c) animal populations as a source of ecosystem disservices, d) the effects of agriculturalisation on FES providers, e) the mechanisms underlying the observed negative impact of provider loss on regulation FES provision, f) the potential condition of regulation FES under future LUCC and g) the expected demand of regulation FES worldwide.
First, we summarise the evidence available to support the FES concept, which highlights animal populations as essential providers of animal pollination, biological control (including pest and disease control) and seed dispersal, as fundamental regulation services operating in both natural ecosystems and agriculture. Hereafter, the topics included in the review are addressed per service, in the order given.
ES provision has been used as a strong argument for biodiversity conservation (e.g.
This is followed by the evidence showing the negative impacts on human well-being that can be produced by animal populations under agriculturalisation, which are referred to as faunal ecosystem disservices (
Animal populations as source of services and disservices. The same ecosystem function mediated by animal populations may enhance (faunal service) or undermine (faunal disservice) human well-being and it can manifest directly (solid arrows) or indirectly (dashed arrows).
Finally, we synthesise evidence indicating the causes of loss of FES providers in response to the consequences of agriculturalisation: landscape homogenisation, habitat fragmentation and loss, microclimatic changes, proliferation of pests and use of pesticides. We describe the impacts of loss of FES providers on provision. It is worth mentioning that we make a distinction between the effects on providers and on provision because the former indicates the causes of loss and the latter its consequences.
Having addressed the present situation of FES and impacts of agriculturalisation, we address the potential trajectories for FES in the future based on the few studies that have used modelling to project agriculturalisation over the next decades and which have also assessed the impact on regulation services. Finally, we assess the expected demand for FES worldwide, given projected population growth and agricultural expansion since service provision cannot be assessed unless changes in demand are understood.
Ecosystem functions can produce ecosystem services (benefits or goods) where there is human demand. A key suite of these services are the regulation services (
The assessment of regulation FES provision is complex, since populations of providers form intricate ecological relationships (e.g.
Most studies in which animal pollination and biological control are evaluated have been carried out in agroecosystems (Table
Faunal ecosystem services. Selected examples of studies where regulation ecosystem services provided by fauna are assessed, describing the providers, ecosystem benefited by the service and service quantification measure.
Ecosystem service | Service provider | Ecosystem | Measure | Study site | Reference |
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Pollination | Native bees | Agroecosystem (watermelon crops) | Pollen deposition | Yolo County, California, USA |
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Exotic and native bees | Agroecosystem (coffee plantation) | Seed mass, fruit set, peaberry frequency, pollen deposition, bee species richness | Finca Santa Fe, Valle General, Costa Rica |
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Nitidulid and Staphylinid beetles | Agroecosystem (atemoya crops) | Beetle species richness | Atherton Tableland, Queensland, Australia |
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Wild bees | Agroecosystem (canola crops) | Bee abundance, seed set | La Crete, Alberta, Canada |
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Ceratopogonids midges | Agroecosystem (cocoa and plantain crops) | Midges abundance, pod set, intercropping proportion | Kubease, Abrafo-Ebekawopa and |
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Edwenease, Ghana | |||||
Hoverfly, solitary mason bee and bumblebee | Agroecosystem (apple orchards) | Flower visitation, fruit set | Reading and Leeds experimental farms, UK |
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Pest control | Parasitoid eggs gs (Mirid bug, Wolf spider, Tetragnathid spiders) | Agroecosystem (rice crops) | Plant- and leaf-hoppers abundance | Luzon, Ifugao, Philippines |
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Aztec ant and Green scale (mutualism avoids occurrence of coffee berry borer) | Agroecosystem (coffee plantation) | Ant activity, green scales abundance | Finca Irlanda, Chiapas, Mexico |
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Great Tits | Agroecosystem (apple orchards) | Percentage of caterpillar damage per apple tree | Netherlands |
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Birds and bats | Agroecosystem (cacao plantations) | Herbivorous insect abundance, final crop yield | Napu Valley, Central |
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Sulawesi, Indonesia | |||||
Birds and bats | Agroecosystem (coffee plantation) | Herbivorous arthropod abundance and leaf damage proportion | Finca San Antonio and Hacienda Rio Negro, Coto Brus Valley, Costa Rica |
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Parasitoid wasps and flies | Agroecosystem (cruciferous crops) | Parasitoid richness, abundance of parasitised cabbage by aphids and loopers | Monterey, Santa |
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Cruz, and San Benito Counties, California, USA | |||||
Leaf beetles, root and flower-feeding weevils | Wetland | Purple loosestrife cover, occurrence of feeding damage and abundance of biological control agents | Minnesota, USA |
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Human diseases control | Mammals, birds and reptiles | Temperate forest | Infected ticks with Lyme disease proportion | Southern New York State, USA |
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Birds | Forested urban to rural areas | Bird diversity, mosquitoes and humans infected West Nile virus | St Tammany Parish, Louisiana, USA |
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Ozark forest, Missouri, USA | |||||
Human diseases control | Small wild mammals | Desert (Caatinga) | Small mammal diversity and abundance, dogs infected with Chagas disease | Amazon Basin, Brasil |
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Tropical forest (Amazon) | |||||
Wetland (Pantanal) | |||||
Rodents | Evergreen forest and Agroecosystem (mainly maize crops) | Infected rodents with bubonic plague abundance | Tloma village, Kambi ya Nyoka village and Manyara region, Tanzania |
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Seed dispersal | Eurasian jay | Oak forest (National Urban Park) | Oak saplings abundance | National Urban Park of Stockholm, Sweden |
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Flying fox | Tropical forest | Flying fox abundance, chewed diaspores | Vava’u Islands, Tonga |
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Thrushes | Temperate secondary forest | Seed abundance and richness and frugivorous abundance and richness | Cantabrian Range, Spain |
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Native frugivore birds | Tropical forest (Wild chillies) | Seedling emergence of gut passed seeds vs. non-gut passed seeds | Guam, Mariana Islands |
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There is a wide range of measures used to assess FES provider contributions to different services (Table
Animal pollination is a fundamental process in terrestrial ecosystems and is essential for maintenance of wild plant communities and agricultural systems (
According to
Given the morphological diversity of plants, the degree of self-compatibility and the diversity of reproductive organs in the flowers of crops, a great diversity of vectors is required for efficient animal pollination (
Biological control is the natural process responsible for the regulation of species’ population growth through ecological interactions –mutualism, parasitism and predation. This has been highlighted as a relevant regulation FES given the key role in restraining the spread of crop pests and diseases (
Predation is one of the best-known mechanisms of biological control for agricultural pests and birds and bats have been identified as the main contributors, by their predation of species responsible for crop damage (
Parasitoidism is considered another important mechanism of agricultural pest control (
Mutualism has been identified as another mechanism that can contribute to pest control.
Disease control is also recognised as a relevant FES (
Animals are also relevant actors in seed dispersal. They drive plant gene flow, population dynamics and spatial structure in undisturbed habitats and contribute to regeneration of deforested habitats, by moving seeds from one site to another (
The ecological value of faunal dispersal is well known (
The economic value of animals for seed dispersal is even less well known than their ecological value (
Some of the studies where the role of animals in seed dispersal has been assessed are in tropical ecosystems.
Species richness (i.e. the number species present in a certain area) is considered the most simple and direct measure of biodiversity (
An empirical literature review by
In contrast,
Regarding regulation FES, there is evidence that, by increasing species richness, FES provision is improved. For instance,
Abundance (i.e. number of individuals per species), rather than species richness, has been suggested as the most important trait that influence FES occurrence (
Some studies have evidenced the relevance of abundance of beetles (
Ecosystem disservices were recently defined as the ecosystem generated functions, processes and attributes that result in perceived or actual negative impacts on human well-being (
For many years, the assessment of the links between ecosystems and human well-being has been focused only on ecosystem services (
The designation as service or disservice depends on the perceived influence on human well-being (
An integrative and balanced approach to services and disservices provides a better foundation for environmental management and conservation efforts (
Faunal ecosystem disservices. Selected examples of disservices related to agriculturalisation caused by fauna, describing providers, type of manifestation: direct or indirect (when causes decrease or loss of a service), category (according to
Provider | Manifestation | Category | Disservice | Reference |
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Invasive pollinators | Indirect (pollination) | Bio-economic | Disruption of native pollinator-plant relationship, spreading of invasive plants |
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Herbivore insects | Direct (herbivory) | Bio-economic | Damage to crops |
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Birds and mammals | Direct (crop riding) | Bio-economic | Damage to crops |
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Invasive hosts | Indirect (disease control) | Bio-health | Novel hosts increase incidence of diseases, decrease of vertebrate population increases the risk of transmission to humans |
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Invasive frugivores and herbivores | Indirect (seed dispersal) | Bio-economic | Disruption of native seed disperser-plant relationship, spreading of invasive plants, emergence of new ecological associations |
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Effects of invasive species on native species are well documented (e.g.
Amongst the reported effects of invasive species on animal pollination services are: the disruption of mutualism between native bees and plants by invasive bees, the range expansion in pollinator-limited invasive plants and consequent distraction of pollinators from native plant species (
Invasive species like weeds, insects and plant pathogens (mainly fungi) can become pests and have major impacts on crops. For instance, a well-documented case is the Mediterranean fruit fly, native from West Africa, but now found worldwide, which causes damage to over 250 types of crops. The cost estimated for California reaches US $1 billion (
Animal seed dispersal can be a disservice when this involves the spread of invasive plants. Just like the service, the knowledge on how animals contribute to the success of invasive plants is limited (
Equally relevant is the effect of invasive species on disease control: invasive plants and animals can act as novel hosts for diseases.
Overpopulation of disease organisms or disease vector organisms and/or the absence of defence organisms can increase the risk of spread for human disease. Many cases of disease outbreaks in human history have been related with invasive pathogens, due to the continual expansion and interchange of human population worldwide (
Native species may also represent a risk for human health if the natural control of population growth is altered or if human contact with vectors increases. For instance,
Since the beginning of agriculture, humans have faced crop pests (
Amongst the known causes of occurrence of crop pests is the imbalance of natural biological control, produced by a change in the abundance of natural enemy populations. For instance, a decrease in predator populations allows the increase of prey population (e.g.
Crop raiding is the term used to describe the action of wild animals foraging or trampling crops (
Literature on this subject is extensive and mostly consists of case studies. The approaches to quantify losses vary considerably and are not comparable from site to site (
The extent of damage varies widely depending on where the raiding occurs and the type of crops and wildlife species involved. For instance, the socioeconomic impact might be higher in developing countries in non-protected areas with farmers losing their livelihood and rarely being compensated for the losses, thereby creating antagonism towards wildlife (
The approaches to estimate monetary losses are variable, varying in unit of measurement and spatial scale. For example,
Human-driven environmental changes strongly influence the occurrence of faunal disservices. Simultaneously, these environmental changes have an adverse effect on faunal services through the negative impact on the providers, mainly caused by the loss or transformation of habitat.
Agriculturalisation is considered to be the main driver of loss, modification and fragmentation of habitats, causing biodiversity loss and ES degradation globally (Gaston et al. 2003,
Landscape heterogeneity refers to the variety of different landscape conditions within a landscape (i.e. area that is spatially heterogeneous in at least one factor of interest,
The inconsistency in the use of terms makes the comparison and synthesis of studies difficult (
The idea that the diversity of landscape components is a key determinant for biodiversity is widely accepted (
A consequence of LUCC due to agriculture is landscape homogeneity, as different land cover and habitat types are converted to more uniform agricultural land. Therefore, the proportion of agricultural land is the most commonly used indicator of homogenisation in studies where the relationship between biodiversity and landscape heterogeneity is assessed (e.g.
Several studies support a positive relationship amongst landscape heterogeneity, species diversity and abundance of FES providers (Table
Faunal ecosystem service providers and landscape heterogeneity. Examples of studies evaluating the relationship of landscape heterogeneity and FES providers richness and abundance, including the definition of heterogeneity as described by the studies’ authors.
Group | Study type | Description of landscape heterogeneity | Relationship | Reference |
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Native bees | Original | Watermelon farms with gradient of agricultural intensification, 1% to ≥30% natural habitat within a 1-km radius | Positive |
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Nitidulid and Staphylinid beetles | Original | Atemoya orchards with gradient of decreasing distance (0.1–24 km) from tropical rain forest | Positive |
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Bees, bumblebees and beetles | Meta-analysis | Isolation of several crops from natural habitats | Positive |
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Coccinellid beetles | Original | Soybean and corn crops with gradient of agriculturally dominated to forest and grassland dominated within a 3.5-km radius, landscape diversity measured as Simpson’s D | Positive |
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Pollen beetles, stem weevils | Original | Various crops with gradient ranging from structurally poor to complex landscape at several spatial scales (250–2000 m radius), landscape diversity measured with Shannon-Wiener index | Mixed (Scale-dependent) | Zaller et al. 2008 |
Leaf-Nosed Bats | Original | Coffee plantations and forest fragments along a gradient of management intensity, landscape diversity measured with Management Index | Mixed (Trophic guild-dependent) |
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Natural enemies of pests | Meta-analysis | Landscape complexity metric consider % natural habitat, % non-crop habitat, % crop, habitat diversity measured using Shannon and Simpson indices | Positive |
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Birds | Original | Coffee farms in sites of mixed cropland and habitat vs. separate areas of intensive agriculture and habitat | Positive |
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Parasitic wasps and flies | Original | Rotatory organic crop fields ranging from homogenous cover of annual crops to primarily forest trees and native shrubs within 500 m and 1500 m radius | Positive |
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Bees and wasps | Original | Historical land cover change using spatial analysis within 1, 2, 5 and 10 km radii | Positive |
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Birds and bats | Review | Cacao, coffee and mixed fruit orchards and tropical forest sites, comparison among forest, agroforestry and agricultural systems | Mixed (Taxa-dependent) |
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Arthropods enemies of aphids | Meta-analysis | Proportion of cultivated land within a 1 km radius around each plot | Positive |
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Wild bees | Original | 50 ha landscape plots in agricultural areas with increasing cover of semi-natural and natural vegetation patches | Positive |
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Butterflies and farmland birds | Original | Proportion of arable field cover | Positive |
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Along with landscape homogenisation, agricultural intensification has led to original habitat loss and concurrently to habitat fragmentation. Habitat fragmentation refers to the reduction of continuous tracts of habitat to smaller, spatially distinct remnant patches (
The degradation of ecosystems by landscape homogenisation, habitat loss and fragmentation results in decreased carrying capacity to sustain all the organisms that inhabit these ecosystems, leading to continued population losses. The loss of populations precedes species extinction and, therefore, the reduction of biodiversity (
Several studies have suggested that the loss of genetically distinct populations globally is both absolutely and proportionally several times greater than the rate of extinction of species (
Habitat loss and fragmentation are the main causes of population decline (
Global declines in pollinator populations are widely recognised (
LUCC causes microclimatic changes in the remaining patches of ecosystem related to temperature, wind and humidity (
Along with climatic modification, physical changes diminish animal habitat suitability by reducing the quantity and quality of nesting, sheltering, and foraging sites (
Environmental changes caused by LUCC may adversely affect biological control processes. Spatial and temporal distribution and proliferation of insects, weeds and pathogens is largely determined by climate, therefore microclimatic changes in temperature, light and water supply can drive overpopulation of pests (
Crop pests produce major losses for crop yields, therefore, farmers have resorted to the use of pesticides as a means of control. In the last six decades, there has been a dramatic increase in the use of pesticides. Along with agricultural intensification, herbicides, insecticides and fungicides have produced highly negative effects on species abundance and diversity (
It is sensible to assume that, by losing populations of providers, the production of ES might be compromised. However, it is crucial to understand the mechanisms that affect provision first. Several studies have evidenced the underlying reasons for the negative effect of population losses on FES production as outlined below.
Regarding animal pollination, the high diversity in morphology and reproductive strategies of plants requires a similar diversity of pollinators (
Equally, a detrimental effect on natural pest control in crops has been identified due to a reduction in natural enemy diversity (e.g. rice crops,
Human disease control can be affected by reduction in species richness. A ‘dilution effect’ (sensu
Seed dispersal is also affected by diversity loss.
In general, even though initial species loss can be compensated by remaining species with similar functions, significant species loss will eventually reduce provisioning of FES. Therefore, to secure FES production, it is essential to conserve species richness.
Along with species richness, population size or abundance, are determining factors for FES provision. Since population losses are higher than diversity losses (
Losses in pollinator populations produce a negative impact in wild plant communities, affecting the integrity of natural vegetation (
Equally affected is the pest control service, where abundance of natural enemies, predators and parasitoid species, largely determines the abundance of species that can become pests (
Regarding the disease control service, population size of hosts has a complex effect on transmission dynamics. Through model-based analysis,
Decline in frugivorous populations reduce availability and quality of seed dispersal services (
Thus, a decrease in abundance of FES providers has a negative impact on FES provision. Even though the reduction is small, the consequences on FES production can be significant given the complex interactions amongst the providers and the ecosystem functioning. Population losses imply more immediate effects than the loss of richness.
While the understanding of the effects of current LUCC on ES provision has increased (
Regarding FES,
Although there is still much to know about the future impacts of LUCC on FES provision, it seems possible to assess changes in supply in relation to agriculturalisation.
ES demand is the sum of ecosystem goods and services currently consumed or used in a certain area over a given time of period (
World population is expected to reach 9 billion people by 2050 and would require raising overall food production by 70% (
Today, the developing world represents more than two thirds of global agricultural production and cultivated land and supports agriculture, which per unit of production, is 50% more pollinator-dependent than that of the developed world (
Human induced changes might increase the demand for natural disease control. For instance, the development of irrigation systems is likely to increase the risk of contracting diseases such as dengue and malaria, by favouring the breeding of vectors, like flies and mosquitoes, in areas where they were absent or rare (
Global forest area is projected to continue to decrease over the next years, although at a lower rate compared with the beginning of the century, declining from 0.13% to 0.06% per year by 2030 (
Ecosystem functions deliver final benefits or goods through the provision of ecosystem services where there is demand for them. To achieve proper management, conservation and valuation of such functions or of regulation ecosystem services and FES, an accurate characterisation is essential and understanding the providers of these services is a significant part. Animal populations are key providers of regulation services and simultaneously can be source of disservices. To secure the service provided and minimise disservices, it is imperative to continue studying their role, to understand the potential implications of their loss and to use this evidence base to advise conservation and sustainable land use.
We identified two components of faunal diversity as influential to FES provision, richness and abundance. Richness brings functional diversity and complementarity, improving the range of FES provision, while a higher number of species improves the magnitude and spatial distribution of provision, since it is abundance that determines the occurrence of these services. Speciose systems with low species abundance may have low or null FES provision.
Animal species may also be a source of disservices to people. We identified invasive and native species pest outbreaks as the most common sources of disservice. Animal populations can be the main actors or can act as vectors of viral, bacterial or fungal pests. The evidence suggests that invasive species can be an indirect source of disservice when disrupting the service provision by native species, while native species may impact directly as crop pests, human disease vectors or crop raiders.
Several studies suggest that agriculturalisation has negative effects on FES providers due to landscape homogenisation, habitat loss and fragmentation, microclimatic changes and population imbalance, causing species and population losses. This increases the occurrence of disservices, impacting FES production through the decrease of functional complementarity — in the case of pollination, seed dispersal and pest control — or dilution effect — for human disease control and increasing crop and disease pest populations and wildlife-human conflict.
Few studies have addressed potential effects of LUCC on FES provision under different scenarios of agricultural change. LUCC models can be used to drive models for current and future FES provision. Such analyses are particularly important given the expected concomitant increase in demand for FES as land continues to be converted for agriculture.
The effects of land use change on FES providers have been assessed mostly at the local scale, using a range of approaches. To improve understanding of these effects at wider scales, it is desirable to develop a common approach to allow comparison and to identify land use configurations that maximise FES provision. For this, further research is required; first, to know the spatial distribution of FES providers; second, to identify the suitable conditions that allow FES providers to provide the FES and third, to relate these conditions to characteristics of land use and cover. Moreover, to date, the different FES have been evaluated independently: analysing them together can provide valuable information about distribution patterns, synergies and trade-offs amongst them.
Conservation prioritisation must factor in faunal ecosystem services (and disservices) as the most biodiversity-relevant of all ecosystem services and those which most closely links sites of conservation value that provide services with nearby sites of service use of agricultural and economic value. This will require the development of spatial models of faunal ecosystem services and disservices to compliment the ecosystem service models in existing tools such as Co$ting Nature (
Maximum robustness of modelling results for policy formulation is achieved by using an ensemble of ecosystem service models, as has been common practice with climate models for decades. Each rigorous new approach to modelling faunal ecosystem services that is globally applicable and inter-operable or capable of comparison with existing models, can be a valuable contribution to improving our understanding of this important class of ecosystem services.
CGA thanks the National Council of Science and Technology of Mexico (CONACYT) for the sponsorship granted for doctoral studies (407586/217401), from which this manuscript was produced. MM was supported in contributions to this as part of the p4ges project (http://www.p4ges.org) funded by the Ecosystem Services for Poverty Alleviation programme (grant code NE/K010220/1).