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Available online at www.sciencedirecl.com --" EUROPEAN JOURNAL Of -.;- ScienceDirect SOll BIOLOGY ELSEVIER European Journal of Biology 42 (2006) S23-838 http://france.elsevier.comldirectlejsobi Original article The values of sail animaIs for conservation biology

a b c b T. Decaëns ,*, II Jiménez , C. Gioia , G.J. Measeyb, P. Lavelle

•Laboratoire d'écologie-ECOD/V, UPRES EA /293, université de Rouen, 76821 Mt Saint Aignan cedex, France b Laboratoire d'écologie des sols tropicaux, lRD, 32, Avenue Henri-Varagnat, 93143 Bondy cedex, France

C Bureau d'élude AL/SE. 228, ZAC de la Forge-Seret, 76520 Boos, France

Available online 21 July 2006

Abstract

It has taken time for the international to accept the idea of values, a concept which had previously been restricted to the limited aesthetic and touristic aspects ofwildlife. This situation changed following the International Convention on Biodiversity in Rio de Janeiro (1992), which focussed on "the forgotten environmental problem" ofbiodiversity erosion and made the first clear reference to the values of living . Biodiversity values refer to direct or indirect, economic or non-economic interest, a given species or may represent for human populations. These values are generally split into intrinsic and instrumental (use) values, the last category itself being divided into direct and indirect economic values. Obviously, each of these values cames different weights, and cannot be considered as being weighted equally in terms of justification for species or ecosystem conservation. Soil is probably one ofthe most species-rich of terrestrial , especially if the defmition is extended to related habitats like vertebrate faeces, decaying wood, and humus ofhollow trees (i.e. epiphytic ). The diversity ofsoil communities (sensu lato) thus probably encompasses a large part of terrestrial animais. This highly speciose fauna has been the subject ofrecent research efforts, and current trends in soil fauna studies include aspects ofbiology, autecology, ecotoxicology, or functional . During the past 20 years, recognition of the importance of soil fauna in the functioning of soils and by extension of terrestrial ecosystems has been continuously growing, ending in sorne important applications in agronomy. However, despite the general agreement about the ecological importance of soil fauna and its economic consequences, the absence of concem about this group from conservationists in their studies is conspicuous. This paper aims at presenting soil fauna within the scope of conservation biology concepts, trying to identify the different values of soil fauna and how they participe to the provisioning of key ecosystem services. Finally, the enormous gap between their recognised usefulness and their consideration in protection policies is discussed. . © 2006 Elsevier Masson SAS. Ali rights reserved.

Keywords: Soil animaIs; ; Biodiversity values; Ecosystem goods and services; Conservation biology; Concepts

1. Introduction touristic aspects of wildlife [29]. This situation has changed, mainly since the International Convention on Tt has taken time for the international community to Biodiversity in Rio de Janeiro (1992), which focussed accept the idea of biodiversity values, a concept pre­ on "the forgotten environrnental problem" of biodiver­ viously associated only with the limited aesthetic and sity erosion and made the frrst clear reference to the values of living species [60]. Biodiversity was at this occasion defined as "the variability among living • Corresponding author. organisms from a11 sources including terrestrial, marine E-mail address:[email protected] (T. Decaëns). and other aquatic ecosystems and the ecological com-

1164-5563/$ - see front matter © 2006 Elsevier Masson SAS. Ali rights reserved. doi: 10.1 016/j.ejsobi.2006.07.001 S24 T Decaëns el al. / European Journa/ ofSail Bi%gy 42 (2006) S23-S38 plexes of which they are a part; this includes diversity tify the different values of soil fauna and how they rely within and between species, and of ecosystems" [63]. on key ecosystem services. The enormous gap between Biodiversity values thus refer to the direct or indirect, their recognised usefulness and their consideration in economic or non-economic interest a given species or protection policies is finally discussed. ecosystem may represent for human populations. Iden­ tifying species values cornes down to answering the 2. How many species in the soil? question: What is a species worth [l3]? These values are generally split into intrinsic and instrumental (use) Estimating the diversity of soil communities values, the last category being itself divided into direct first requires a definition of a "soil animal". Wolters and indirect economic values [29,52,66,106]. [129] distinguishes between the "full-time inhabitants" Obviously, each of these values carries different (many micro- and mesoarthropods, and weights, and may not be considered equally powerful macroinvertebrates) and the "part-time inhabitants" of in terms of justification for species or ecosystem con­ soil (Iike many vertebrates, soil dwelling larvae servation. or mound-building ). But what about species that Soil is probably one of the more species-rich habitats mainly live in/on the litter layer like for example Car­ of terrestrial ecosystems [129]. If extending the defini­ abidae predators? Where does soil began and end? tion of soils to related habitats like vertebrate faeces, What about vertebrate dung, decaying wood, rocks, decaying wood, humus of hollow trees, the diversity hollow trees and other "epiphytic" soils; ail habitats of soil communities (sensu lato) probably encompass termed "soil annexes" by Gobat et al. [54]. In this the majority of terrestrial animal species. This highly paper we adopt a sensu lato definition of soil animais speciose fauna has been the subject of recent investiga­ and will take into consideration examples from these tion efforts, with current trends including biology, aute­ habitats highly connected to the soil sensu strito. cology, ecotoxicology and . During Soils probably represent a necessary substrate for a the past 20 years, the recognition of the importance of large part of global biodiversity. For example, the soil fauna in the functioning of soils and by extension majority of animais in terrestrial habitats are soil inha­ of terrestrial ecosystems has been continuously grow­ bitants for at least one stage of their life cycle [7,129]. ing, ending in sorne important applications in agronomy A rapid survey of invertebrate and vertebrate groups (see e.g. [82]). reveals that at least 1/4 of described living species are Despite the general agreement about the ecological strictly soil or litter dwellers, the main part of which is importance of soil fauna and its economic conse­ insects and (Fig. 1). This prodigious below­ quences, the absence of concem about this group from ground diversity le

Vertebrata Annelida <1% Microinv 1% 2% Bacteria and Fungi 4% virus <1% Otber Arthropoda 5%

Other Insects AnimaIs 80% 55% SoU animaIs 23% (i.e. - 360,000)

Total number of described living species: - 1,500,000

Fig. 1. Importance ofsoit animaIs for the global biodiversity (a) and relative importance of major taxa wilhin soil communities worldwide (b) (data from [27,68,104,120,124]). T. Decaëns el al. / European Jal/mal ofSoil Biology 42 (2006) S23-S38 825 of coexisting soil dwelling species [127]. A set of con­ microarthropods. AdditionaIly, even for higher body­ cepts and ecological theories are proposed to explain sized groups for which the taxonomic knowledge may this pattern [33,85,118], involving local processes shap­ be higher, basic species biology, ecology and distribu­ ing the interactions between individuals and popula­ tion patterns remain unknown (see e.g. [50] for earth­ tions, such as trophic niche partitioning, spatial and worms). temporal segregation, relaxation of density dependant To explain this major drawback in soil biodiversity regulations by adverse soil conditions, and a high diver­ knowledge, authors generally stress the lack of taxo­ sity of micro-habitats [53,129]. AIl these rnechanisrns nomic expertise [4,11,23,53,124] and of standard sam­ are probably favoured by the of the physical pling methods and protocols [5,23,93]. AIl this deserves environment, as the three-dimensional structure of the much effort in methodological and taxonomic knowl­ soil, the wide range of pores, surface types and micro­ edge to allow meaningful estimation of cIimates, may reduce competitive exclusion and pro­ in soil communities, its main patterns and how it affects mote greater species coexistence through par­ soil processes and ecosystem functioning [5,23]. titioning. Despite its supposedly critical contribution to global biodiversity, soil fauna has received compara­ 3. The intrinsic values of species tively iittle taxonomic attention when compared with other groups such as higher plants and vertebrates. To Many conservation biologists believe that every spe­ date, in many groups, there is a considerable imbalance cies has intrinsic values, i.e. values not related to any ofknowledge oftropical and temperate species, reasons economic or other aspect of usefulness [52,66]. This why the soil community has been referred as the "Poor conception mainly ensues from ethical considerations, man's rainforest" by Giller [53], and as a new biotic from which emerges the idea that a species has value frontier [6,60]. In fact, the more optimistic estimates without reference to anything else but its own exis­ suggest that soil and leaf litter richness is tence. This value recognises its cultural, social, aes­ about five times larger than in the canopy [91,117]. thetic, and ethical benefits. High social and religious Fig. 2 presents an overview of the number of values are attributed to individual species or commu­ described species vs. the estimated number of species nities of organisms by sorne groups in society. that remain undiscovered for the major taxa of soil ani­ Secular and religious standpoints often allow a spiri­ mais (modified from [124] with additional web tual value to each species, maintaining that people have sources). In general, the smaller the taxa are, the more a moral responsibility to protect earth's wildlife [47,52]. they are disregarded in biodiversity surveys (but see Early in the last century this thinking constituted the [93]). This synthetic figure corroborates conclusions intellectual framework of the political conservation of André et al. [5] who estimate that the ratio of 'num­ movement of John Muir (1838-1914). While Muir ber of described species/number of existent species' wrote about the equality of species in religious terms, converge on values inferior to 10 for most groups of the ecologist Aldo Leopold (1886-1948) was probably

o Estimated undescribed species .Described species

!@ 1000

100

10

Fig. 2. Estimated numbers ofdescribed and un·described species for major soil animal taxa (data from [124], various web sites); NE = no estimation available. S26 T. Decaëns el al. / European Journal ofSail Biology 42 (2006) S23-S38 one of the first scientists expressing equality in ecolo­ humans [109]. In Amazonia for example, at least 32 gical terrns and questioning the well-founded species ethnie groups consume a significant amount of small utilitarian perspectives (see [66]). He argued that the terrestrial invertebrates, and the total number of edible study of the multiple functions played by any given invertebrate species used as food in this area is more species in an ecosystem is a so complex task that no than one hundred [100,102]. The variety of inverte­ man can say where utility begins or ends [88]. Leo­ brates that have been adopted as food is impressive pold's works were the basis of an evolutionary­ and include numbers of soil inhabitants, including geo­ ecological ethic that considers the importance ofpreser­ phagous, detritivorous, saproxylophagous, leaf cutters, ving species as unique evolutionary links and functional predators and generalists [100]. Among the more elements of ecosystems. wide1y used soil animaIs figure leaf-cutting ants (For­ Accepting the idea of species having an intrinsic micidae: Atta sp.), litter-consuming termites (e.g. value is still highly useful in conservation biology Synthermes sp.) and earthworms (e.g. Andiorrhinus because of its simplicity and equity. As this value is sp.) [102]. by definition the same for ail species, assigning a con­ Examples of local populations consuming soit inver­ servation status to a given plant or animal species may tebrates are currently reported in the literature. Entomo­ thus be done using extinction probability as the more phagy (including root feeding Lepidoptera larvae and relevant criteria. different ant species) is for example particularly impor­ tant in the culinary culture of Australian Aborigines, 4. The instrumental values of species and in many cases concerns soit insects [59]. In Co10m­ bia, native habitants of the Orinoco Llanos are very Instrumental values refer to the effective or potential fond of swarming females of Atta laevigata, locally use of species by human populations [66]. The ways of named "culonas", which they consume like peanuts using wild species are diverse and allow conservation after toasting the large abdomen in its own butter (TD biologists to assign different kinds of instrumental and JJJ, personal observation/tasting). In sub-Saharan values to biodiversity. On an economic basis, soil Africa, termite alytes are a highly prized foodstuff and fauna has both direct (the organisms themselves and! are fried in their own oil with salt to produce a delicious or their metabolic products) and indirect (the long­ and nutritious snack (GJM personal observation/tast­ terrn outcome of their activities) uses. Direct economic ing). In Venezuela, the Ye'Kuana ethnie group collect values are assigned to species that are directly har­ and consume at least two different edible earthworrn vested; e.g. for food, fuel, recreation. Indirect economic species locally called "motto" and "kuru" and recently values refer to aspects of biological diversity such as described under the name of Andiorhinus motta and ecosystem processes and environmental services that A. kuru [101]. provide economic benefits without being directly har­ In many indigenous populations, the use of edible vested [106]. soil invertebrates corresponds to an important strategy that takes advantage of a highly abundant and renew­ 4.1. Direct economic values ofsail animais able resource [59,102]. Invertebrate consumption can provide significant amounts of animal proteins, espe­ Direct economic values are probably the easiest to cially during difficult periods of the year (e.g. rainy evaluate by observing representative groups of people seasons) during which fish and game is scarce (e.g. and market activities from a local to international scale. 60% ofanimal protein diet during rainy season for Gua­ Primack [106] distinguishes consumptive use values jivos Amerindians of Venezuela). (i.e. goods that are consumed locally) and productive use values (i.e. products sold in markets). 4.1.2. Productive use values In a few cases, soil animais used as food may be 4.1.1. Consumptive use values found in local markets. This is the case for The use of soil animais as protein source in human A. laevigata in Colombia, which is sold at 1-1.5 Euros nutrition is still widely represented in indigenous popu­ 100 g-l during the swarming season in the street of lations in most regions of the world [42,43] and was Santafé de Bogotâ and other large towns of the country first reported by Wallace [125,126] more than (Bonilla pers. corn.). Smoked earthworrns consumed by 100 years ago. More than two thousand invertebrate Venezuelan Ye'Kuana also has a high commercial species are utilised worldwide as a food resource by value in local markets, three times higher than the T. Decaëns et al. / European Journal ofSoil Bi%gy 42 (2006) S23-S38 S27 price of smoked fish, game, pork or chicken [101]. In tude of difficulties mainly due to the dietary plasticity 1981 in Mexico, the demand for "escamoles" (imma­ of many soil animais [113]. New molecular methodol­ ture stages of the ant, Liometopum apiculatum Mayr.) ogies (e.g. fluorescence in situ hybridisation, natural was so great that the price per kilogram went up to variations in stable isotope contents in animal tissues) 1000 pesos (>1.5 Euros at the then- prevailing have recently given this discipline new and highly rele­ exchange rate) [43]. vant perspectives (see review by [113]). An alternative A high number of coleoptera species, which larvae and relatively recent approach is to focus on the impact live in the soil sensu lato (mainly rhizophagous, saprox­ of species on their physical environment through a ylophagous and predators), are currently sold at insect 'functional domain' approach [3,77,78]. Functional fairs and specialised internet markets. A proportion of domains are defined as the sphere of soil influenced this business concerns scientific material, which is char­ by the activity of a single species, in which important acterised by a high number of specimens generally sold soil processes are regulated and resources for other soil to museums or private scientists at relatively low prices. biota indirectly modulated [78]. This approach has pro­ Other specimens are prized for their ornamental interest ven its usefulness to address the functions of the so to make decorative elements (e.g. Rutelinae, Cetoninae, called 'ecosystem engineers' (sensu [71]) or 'bioturba­ Carabidae etc.). Finally, the larger and/or more charis­ tors' (e.g. earthworms, ants, termites), which interact matic species may be sold to collectors, even as dried with the soil community through trophic, but also and adults of live stock, sometimes at extremely high prices above ail atrophic (engineering) relationships. A just as for the more spectacular individuals of some giant a recent attempt to integrate these complementary con­ Dynastinae or Cerambycidae species or sorne colourful cepts has proven its usefulness in drawing conceptual Rutelinae or Cetoniinae species (arround 2000 Euros). diagrams of interaction webs between above and bellow This particular productive use value is directly propor­ ground biota (Fig. 3; [22]). tional to the aesthetical value of the species. Soil functioning is mainly controlled by a suit of factors ranging from abiotic with large scale domains 4.2. Indirect economic values (climate, mineraI substrate) to biotic with smaller scale domains ( and soil biota) (Fig. 4, [80,121]). Indirect values, although more difficult to evaluate At this last scale, soil animal communities are impli­ from a monetary point of view, may in sorne cases be cated in most key . Organic matter extremely important to support economies. If the ser­ dynamics, nutrient cycling, C storage, , vices related to these values are not performed, substi­ water and storage in soil are mediated by tute resources must be found, often at great expense. soil biota, wich therefore contributes to the maintenance ofecosystem integrity [22,23,60,77]. Many ofthe func­ 4.2.1. Ecological values and ecosystem services tions performed by soil animais rely on important eco­ Ecological values of soil animaIs refer to the way system services at scales orders of magnitude above this biota provides ecosystem services via ecological that of the organisms and their functional domains functions. Part of this functional significance may be (Fig. 5; [3,7,79]). The only service of organic matter of direct utilitarian value for humans in the production can be considered of maximum concern of goods and services that can be priced. Beyond this as 60-90% of terrestrial is decom­ lie a range of ecosystem services that are of acknowl­ posed in the soil [53]. Available literature relating the edged benefit to humans but which generally lie outside functional importance of soil animais as mediators of the boundaries of recognised utilitarian benefit. Tt is ecosystem services provides growing evidence that probably one of the more documented aspects of soil without soil biota, ail terrestrial ecosystems would col­ animal values. lapse rapidly [60]. Ecological functions of soil animaIs have been Finally, soil animais also constitute a food resource widely addressed in the scientific literature, and func­ for many animais and hence feed a species-rich com­ tional classifications have been proposed by different munity of predators [56,60,86]. Earthworms constitute authors. Sorne of these classifications, based on trophic for example a keystone resource consumed by more relationships between species, are mainly issued from than 175 species of mammals, birds, reptiles and models [12,127]. studies allow amphibians in France [57]. In addition to these groups, the aggregation ofspecies into guilds according to their predators preying upon earthworms may be found in a , although this approach inherits a multi- wide number of taxa, including fishes, insects (mainly S28 T Decaëns el al. / European Journal of Sail Biology 42 (2006) S23-S38

Aboveground _ Aboveground ~predators

LiJler comminulioll Litter and soif ~ Litter predators/ /'" engineers ,--- -,

! Root feeders

Fig. 3. Conceptual model of soil interaction web involving the main functional groups of soil animais and their relationships with aboveground biota. Dark arrows: trophic interactions; grey arrows: enfineering interactions; dotted arrows: feed backs (after [22]).

Climale Climare Minera! subslrare MineralslIbstTate -;" -;" ~ Topography ~ Topography -; Agricu/lura/ practices -; Agricuftura! pracrices <: '.c Vegetation Vegetalion '"~ '"~ OD OD .~ Foodwebs .~ Foodwebs Fune/fonal dornains Funclional domains "...'" "...'" .e" " Soil sfmc/ure [ormarion .e Soif sfrucrllre!ormation OMdynamics OMdynarnics

Increasing time scale Increasing time scale

Fig. 4. Hierarchical model of the factors controlling soil functioning Fig. 5. Hierarchical model of the impact of microscale faunal­ (after [40,80]). mediated processes on large scale ecosystem processes and emerging goods and services (after [40,80]). Coleoptera), myriapods, gasteropods, , shelled slugs, , opiliones, dipteran larvae [86]. In a more [66]), which is generally related and proportional to the applied domain, soil invertebrates have been considered subjective notion of species "aesthetic" values. Thus, to be of potential use for domestic animal nutrition [56, although obviously of lower importance when com­ 57,59]. pared to more charismatic groups like tropical forest vegetation or large vertebrates, sorne tour operators 4.2.2. Patrimonial and recreational values often exploit the high diversity of soil invertebrates. Many people throughout the world care about wild­ In tropical America for example, an increasing number life and are concemed with its protection, thus confer­ of countries provide "insect hunting tours" in which ring to species or ecosystems a high "existence value". collectors are invited to collect their favourite families, People value these feelings in a direct way by joining including a number of soil dwelling taxa (mainly and funding conservation organisations that work to Coleoptera and Arachnida). protect their favourite species or habitats [66,106]. More indirectly, sorne vertebrates that prey upon soil This can represent enormous amounts of money when fauna may represent a particular interest for human applied to representatives of the so-called "charismatic populations, either because of their potential use as megafauna", but there is little or no evidence that the game or, conversely, because of their presence on red same occurs for soil animais, i.e. what is the attractive­ lists of threatened species. The importance of soil ness of a soil species to the general public? macrofauna resource for declining bird and amphibian Sorne tropical countries however are actually taking populations has been suggested by Haskell [61] for the advantage of their high biodiversity to develop eco­ forests of the Southem Appalachian Mountains. In tourism. This local economy has its roots in an increas­ France Granval [57] also underlined the importance of ing interest for wild plants and animais (i.e. biophilia, as food resource for 63% of small T. Decaëns et al. 1European Journal ofSail Biology 42 (2006) S23-S38 529 game in France, and as an important factor for sustain­ (): a medium sized Eurasian that is ing specialised predator populations like woodcock used as a by conservation biologists (Scolopax rusticola; Scolopacidae). Re also provided and may help with conservation ofold European hedge­ a list of 114 vertebrate species of the French fauna rows that hoId partieularly speciose plant and animal that consume at least occasionally earthworms, 94% communities (see below). of which have sorne kind of legal protection ( Many groups have been used as indicators of the of bird directive from the EC, Bonn or Washington level of caused by human activities. Differ­ conventions) and more than half are listed on mCN ent groups of soil invertebrates have also proven to be red lists [49]. useful in this domain, like e.g. Nematoda [19], Collem­ bola [105]. Soil macroinveretbrates comprises ofa large 4.2.3. Scientific and educational values range of taxa with diverse biological and ecological A set of concepts and ecological theories are pro­ traits and patterns of response to different kind of posed to explain the extreme1y rich diversity in soils anthropogenic perturbations [99]. Macroinvertebrate with the advent of that is progressively communities thus provide an accurate and relevant making its way and becoming a truly interdisciplinary view ofecological risks that integrate a number ofpara­ field of scientific innovation [33,85,118,127]. For meters like e.g. soil physico-chemical conditions, bio­ example, one of the theories that relate the activities availability of pollutants across time, etc [15,20,44,51, of soil macrofauna and the trigger of 85,89,95,112,122]. depending on these activities has been explained by using the "sleeping beauty paradox" [76]. Besides, stu­ 5. dies on the behavioural ecology of ants and termites have resulted in the development of theories that have served as models in social studies, by comparing how The emerging discipline of ecological economics their societies are organised with those of humans. [35,103] considers the full range ofservices that society With reference to education, it is weil worth men­ derives from nature, because ecosystems provide ser­ tioning the importance of informai education, such as vices that are non-extractive and sorne methods have "Farmer Field Schools" or schools without walls. It is a been developed for valuing such services, even when learning-by-doing process for both farmers and scien­ these are not included in conventional markets. The tists working with them. The impact ofthis process was inclusion ofthese non-extractive services changes dras­ revealed in the rice fields of South East Asia where by tically the outcomes of the economic analyses [62,65, using this approach a reduction of 60% in the use of 123]. pesticides led to increases in rice production and sus­ One step is to identify and describe the values ofsoil tained [90]. Or in the case of edu­ organisms, but an important aspect is to evaluate these cation for children, for example, web sites functions from a monetary point ofview. Rence, ifbio­ or journals (where a "soil wizard" guides children to diversity could be assigned an economic value, it would discover the secrets of soil (see [96,119]). provide very strong arguments to conservation biolo­ gists to justify biodiversity protection towards politi­ 4.3. Strategie values in conservation biology cians or policy makers [13]. The total economic value of a given ecosystem may be considered as the sum of From a conservation point ofview, it is interesting to the different values listed in this paper (Fig. 6; after compare the ofspecies and the range oftheir [106]). impacts on ecosystem functioning. Rence, it is possible Obviously this task is one of the more problematic to rank, by increasing levels of conservation priority: as many values listed so far are indirect and difficult to common, dominant, rare, regulating and keystone spe­ express in economic terms. Intrinsic species values, for cies [106]. Another view is to focus on the strategic example, are by definition devoid of any economic potential ofspecies rather than on their ecological func­ values, and thus williack persuasive power to be really tions. "Flagship" or "" are charismatic useful. Conversely, sorne ecological values will be of species with large geographic and/or habitat range, high indirect monetary importance, especially in agri­ whose protection benefits a large number of non­ cultural soils where animais will participate to culti­ targeted species. One of the rare examples in soils is vated plant through their impacts on soil provided with the scarabid beetle eremita fertility [81]. 530 T. Decaëns et al. / European Journa/ ofSoil Bi%gy 42 (2006) S23-S38

Total economic value Environmental factors are known ta shape living community structure through ail spatial domains, from Present Instrumental values Existence and Option values patches to landscape and biosphere. Following this strategie vll.1ues Future products: · ProloclÎng biodiversity - Food resources Direct cconomie idea, the "species pool hypothesis" considers local spe­ Indirect «onomie · MllinlD:ining culture of - Genelic resources values values local people . Medicines cies diversity as a subset of a regional species pool (i.e. - Food rcsources - Ecosyslcm services · Conlinuillg ecological . Specics for spetialised - Recreation and lourism and Cvolul;onary the number of species potentially present in a given markets - EducDlion proccsses region) [1,17]. Biodiversity driving factors act as envir­ { cconomic estimation Increasing difficulty 0 onmental filters, removing species from the original pool at different spatio-temporal scales according to Fig. 6. Conceptual scheme of the global economic value of sail their biological traits [1,73]. The impact of anthropic biodiversity in a given ecosystem (after [106]). activities on community diversity may thus be consid­ ered as a result of modifications of these natural filters, 6. Threats on soil fauna biodiversity or of the creation of new filters. This may occur even at the local scale (i.e. changes in biotic interactions Species vulnerability to extinction mechanisms is a through e.g. modification of the vegetation or introduc­ function of several factors including species adaptive tion of exotics), the ecosystem scale (i.e. ecosystem strategy, individual abundance, geographic range and alteration or conversion to agro-ecosystems), or larger specialisation for a given habitat [66,106,107]. An scales (i.e. landscape fragmentation, global change) important point is that most of these species attributes (Fig. 8). are likely to be interdependent, as demonstrated by the general positive relationship between abundance and 6.1. Local scale jilters: exotic plantations and invasive geographical distribution [21,52], which seems to also species apply to soil invertebrates [129]. Species with narrow geographical ranges tend to have small local popula­ Introduction of exotic species into ecosystems is of tions, making them more vulnerable to extinction by major concem for conservation biologists [66,106,107, increasing the likelihood ofstochastic and simultaneous 124]. It may have severe impacts on soil biodiversity by extinction [106]. In a recent contribution on Amazonian altering the biotic and/or abiotic environment, or by fauna, Lavelle and Lapied [83] (Fig. 7) stressed the fact modifying competitive interactions within communities that earthworm and, to a lesser extent ants, present a (i.e. the finer-scale filters on Fig. 8). Here we discuss very low local to regional richness ratio when compared separately the impact on soil fauna communities of the to many other invertebrate groups. This means both deliberate introduction of plants for agricultural pur­ taxa may comprise of a high proportion of geographi­ poses and of the often accidentai introduction of inva­ cally restricted species, suggesting that there is a high sive soil animais.' proportion of still undescribed species with a high risk Contradictory examples of the impacts of cultivated of extinction under anthropogenic factors. plant introduction may be found in the literature. In the tropics Eucalyptus spp. produce a poor-quality litter [14] that has detrimental impacts on soil macrofauna 'J> 'J> 80% especiaUy in young forest stands (e.g. tennites; [92]). ..c'" u" .:: In temperate North America, the introduction of Ber­ ëü 60% beris thunbergii and Microstegium vimineum modifies "0 'iio 40% soil pH and organic matter levels, thus increasing earth­ :5'" os worm density and, subsequently, soil porosity [75]. u B 20% Conversion of the Amazonian forest inta pastures ~ sowed with introduced grasses and legwnes is also 0% ~ ~ V> l1 ~ ~ -5 0. Ki ., known to eliminate native fauna which is thus replaced 0 .D'" :q ~ '" '" ê ê ê0 ~ ~ ~ by exotic [30]. On the other hand, ~ ê 0 ~ .><= t:: Oll" .c Oi f-" :> ~ bb'" ci ça 1:! t: similar pastures in Colombian savanna areas have :r'" .E: 0 CI ~ Vi '" been found to conserve native soil communities [41, 70]. Fig. 7. in different Amawnian invertebrate groups, calculated as the ratio between regional and local species richness Exotic species dynamics in soil fauna conununities (after [83]). have been little investigated, although examples are T Decaëns el al. / European Journal ofSail Biology 42 (2006) S23-S38 53l often quoted in the literature. Lee [87] reports more is driven by the productivity level and the perturbation than 100 species of exotic earthworms worldwide, and rate of the considered ecosystem (Fig. 8). The maxi­ Fragoso et al. [50] listed more than 50 species in tropi­ mum diversity is observed in systems where equili­ cal regions. Introduction of exotic macroinvertebrates is brium exists between both factors, whereas local spe­ generally followed by significant impacts on corhmu­ cies extinctions may occur by lack of demographic nlties or soil functioning [85,124]. For example, the recuperation when perturbations increase or by compe­ expansion of the invasive earthworm species Amynthas titive exclusion when productivity increases. hawayanus (Megascolecidae) in New York forests has Disturbance associated with prac­ been reported to generate deep modifications in soil tices are extremely diverse, going from decrease in organic matter composition, water infiltration patterns refuges or trophic resources in case of firewood har­ and [24]. In soils ofthe , vesting ([59,97]) or modifications of soil microclimate northern and United States the invasion of exo­ following periodic fires ([25,34,41,55]), to high mortal­ tic has led to an increased preda­ ity of soi! fauna consequent!y to tillage or use of pesti­ tion pressure on native earthworm species [18,98] In cides ([37,38,41,45,46,84,110,116]). System carrying Amazonian pastures, forest endemic-earthworms lar­ capacity for soil fauna is generally highly increased in gely disappear and are rapidly replaced by monospeci­ medium intensified systems, e.g. sowed pastures. Earth­ fic populations of Pontoscolex corethrurus (Glossoseo­ worms particularly take advantage of these suitable lecidae), a peregrine earthworm which causes severe condition to rapidly dominate communities [9,38,41, compaction in surface soil [30). On the other hand 70,84). Converse!y to pastures, many tilled systems Lee [87] also pointed out the potential functional inter­ are characterised by a decrease in organic matter levels, est of peregrine species in agricultural lands where which leads to a weak potential of population growth native species have disappeared. and higher probability of extinction process when dis­ turbances are increased by practices [39]. 6.2. changes and agriculture intensification Land use changes and agricultural intensification also generate severe habitat degradation or destruction Conversion of natural vegetation into agroecosys­ for soil biota. In many cases, is tems and agriculture intensification, have profound reported to have negative impact on soil fauna [8]. impact on soil communities because they involve Examples include: the reduction in soil macrofaunal changes within the primary determinants of soil biodi­ biomass associated with regular movement of workers versity, e.g. vegetation and soil microclimate [39,124] in Indian tea plantations [) )4]; the impact of sheep and (Fig. 8). As stated by Decaëns and Jiménez [39], agri­ goats compacting soi! on South African subterranean cultural intensification impacts on soil animal diversity herpetofauna [10]; or the detrimental effects on soil fits weil within the Huston's dynamic equilibrium macrofauna of large logging equipment, tractors and model [67). According to Huston, community diversity other vehicles [108). is another severe pro-

Emerging Human patterns Environmental filters Scales impacts

'"ma•• • Cümatic changes Biogeographie distributwn .-Large scale ero!Jlon Loeal mechaolsms -;;.. distribuJion ~ .- ~~~t1~m~; :;;;:;::;~...... Land use changes (jj.... o DispermJn ; . LANDSCAP.E Cl. 8 lAnd use piâetiees • Managemenl practices .. SurvivaJ ~~M~!ll;>" .E,COSYSTEM ....-- ~ E:«IIt~n "" mechanisms _ Introduction ofexotic species Coe.ristence ~~..... PATCH ....-._~

COM~tuNITY ) Spatial scale

Fig. 8. The species pool hypothesis or how environmental factors act as filters that detennine the composition and diversity ofcommunities from a large scale species pool (after (1 D· S32 T Decaëns el al. / European Journal ofSoi! Biology 42 (2006) S23-S38 blem associated with agriculture in many corners of the communities are not likely to be restored easily [85, globe [72], leading to a total destruction of soil biota 124]. habitats. \\Then surveying the contents of major conservation At larger scales, impacts of land use modifications biology journals ([16,48,74]), we found that papers and agricultural intensification may be observed from dealing with soil fauna only represented 8% of the the landscape to the global levels. As an example, papers dedicated to animal taxa (Figs. 9, 10). The over 50,000 different pesticide products, representing most addressed soil taxa was ants with 239 papers, a weil over two million metric tons are used each year number far below that of papers dedicated to vertebrate [66], with non-target impacts extending beyond the groups. A similar trend was found when 100king at soil local scale via processes along the animaIs in the red lists of the IUCN [69]. Less than 100 whole soil food web and eliminating natural predator species are considered threatened to any degree, and insects of certain pests [26,36,66, 111,128]. Although soil animaIs only represent about 1% of the total num­ the subject has been little documented in the Iiterature ber of listed species (Fig. II). Only eight soil animal for soif biota, natural and land­ species have CITES protection world-wide (i.e. three scape structure have been shown to be important for scorpions, four tarantulas and one lucanid beetle [28]). both macroinvertebrate density and diversity [31,32,61]. This point constitutes a real paradox if we consider the high number of species that can be found in insect fairs in many European countries. 6.3. Atmospheric CO levels and climate change 2 As a consequence, soil animaIs are not taken into account in preliminary biodiversity surveys that are Climate change, increasing atmospheric CO2 levels, undertaken for protected area planning. At the local and the resulting changes in rainfaII patterns, soil tem­ scale, impact studies necessary prior to the establish­ peratures, and plant perfonnances are predicted to alter ment of any kind of infrastructure do not consider soil soil fauna through different modalities according to the taxa (Gioia pers. observation). This is also the case considered scale [118]. Hence, the geographical distri­ when similar studies are needed to define the place bution of soil species is likely to be indirectly influ­ and shape of natural parks and reserves (e.g. in Uganda enced through changes in vegetation distribution [58, [64]). This is still obvious when biodiversity spatial 124,129]. Ecosystem-level effects of elevated CO2 are patterns are addressed for the identification of proprie­ expected to be indirect rather than direct because most tary conservation areas at larger scales (e.g. biodiversity soils have higher CO2 concentrations than surrounding hotspots; [94]). Many impact studies particularly lay air due to root respiration. Indirect effects on soi! biota emphasis on higher plants, vertebrates and, among may occur from changes in plant metabolism, resulting invertebrates, on butterflies and to a lesser extend on in modification of litter quality and reallocation of C moths. and N [85,124]. Although still largely misunderstood, In few cases are soil organisms used in impact stu­ responses of soil fauna are likely to be different among dies which result in significant decisions at the local ecosystems. Swift et al. [118] suggest for example that Physical cold-limited arctic ecosystems are particularly sensitive elimination to global warming, while nutrient limited temperate grasslands are susceptible to CO2 increase and N­ depositions.

7. Current status of soil animais in conservation policies

Giller [53] stressed the conspicuous lack of attention ~ Competitive paid to soil biota by conservation biologists, and ~ exclusion described the soil cornmunity as "the poor man's tropi­ cal rain forest". This opinion was recently followed by Resource availability and quality (potential growth rates of populations) Wolters [129], who considered the lack of conservation ecology approaches for soil biota as a major shortcom­ Fig. 9. The Huston's model of diversity driving factors at the ing of . Paradoxically, soil habitats and their community level [67]. T. Decaëns el al. / European Journal ofSail Biology 42 (2006) 523-538 S33

1600 T7.Wl"------;=====::::::;s:=o;::n===='-1

1400 Invertebrates 8% ~ 1200 Other ... invertebrates "Q. 15% 2. 1000 ~ o ~ 800 ,Q ~ 600 z: 400

200 o

Fig. la. Number of papers published in three biological conservation joumals according to the considered taxa (data from [16,48,74]). scale. ln France for example, the discovery of the beetle 8. Conclusion and perspectives 0. eremita, registered in 1979 and 1992 in annex II of the Bern Convention "Habitats" Directive, during ento­ The multiple values of soil animais presented in this mological surveys prior to a road construction justified paper provide good arguments to justify concerns about the suspension of engineering works over more than decreasing soil biodiversity. Hence, soil biodiversity 3 years. Taking into account this species while redefin­ ensures the multiplicity of the ecological, environmen­ ing land organisation significantly orientated manage­ tal and instrumental functions of soil animais in a wide ment decisions at different scales. For example, the variety of environmental conditions [129]. Policy conservation of individual old hollow trees and the makers, the public, and national and international maintenance of hedgerow networks as ecological corri­ trade and economic organisations have yet to realise dors. These protection actions obviously helped at con­ that soil biodiversity is linked to the visible above­ serving populations of 0. eremita, but were also con­ ground compartments of ecosystems, and contributes sidered beneficial for a number of species associated to ecosystem services and goods that drive economics with temperate hedgerows, inciuding a number of and benefit humanity [85,124]. plants, saproxylic invertebrates and fungi, noctumal As pointed out by Bengtsson et al. [12,13], the rela­ birds, bats and oilier small-mammals. tionships between biodiversity and ecosystem function-

Other invertebrates Miriapoda 7% 17% 1%

Squamata 21%

Caecilians 2% Plants 51 % Total number of listed species: 11150

Fig. Il. Relative contribution ofsoil fauna in the lUCN Red Lists of threatened species (a), and relative representation of the major taxa within the threatened soil animal species (data from [69]). S34 T. Decaëns el al. / European Journal ofSoi! Bi%gy 42 (2006) S23-838 ing, far from being simple, appears to be system­ nificant ecosystems goods or services (regulating specific, taxa-specific and process-specific in the light species), or are sufficiently charismatic to be used of our CUITent knowledge. In soil while the number of as umbrella species by conservation biologists. We functional groups of animais is important, the number also need to identify strategic habitats for conserva­ of species per se does not affect primary productivity tion below ground biodiversity hot spots or ecosys­ [115]. Even if the functional importance of soil biodi­ tems that sustain key ecosystem services at the land­ versity still lacks sufficient studies to be clearly under­ scape scale (keystone ecosystems). stood [127], its conservation is vital as an insurance • How can we transfer our scientific knowledge to the against unpredictable or expected environmental public, policy deciders and soil users? Protection and changes that may impair ecosystem functioning in the conservation ofsoil biota will necessitate and justify future [13]. Yet evidence suggests that the destruction more education on the role of "subsurface" habitat ofsoil and its biota would result in cascading effects on biodiversity and how they are linked to aboveground ecosystem biodiversity and functioning, thus impairing organisms [85,124]. Elementary biology curricula their capacity at maintaining ecosystem services [85, should include more comprehensive approaches to 124]. In other terms, the application of the so-called understand how ecosystem functions are sustained "precautionary principle" suggests to consider the con­ by biotic interactions, and how the relationships servation of soil biodiversity in planning and policy between biota and the complex physico-chemical making. soil environment are important to regulate key pro­ We propose the following questions and sorne cesses like nutrient cycling and organic matter related research perspectives as main challenges for decomposition. future soil ecology research: Finally, the "option value" of soil animais, which • How many species in the soil and which functions do they assume? Soil ecologists need to develop refers to their potential to provide an economic benefit strategies to increase the number of taxonomists to human society at sorne point in the future [106] and systematists working with soil taxa, as they are should also be considered in further studies. This future presently very few [85,124]. They also need to better value is hard to predict, since it may be based on pro­ understand the basic functions assumed by these ducts or processes that are as yet unimaginable. To organisms, especially for poorly studied taxa. date, no attempt has been made to address this topic • How much soil biodiversity is enough to maintain for soil fauna. Though, the option values of soil animais the integrity of ecosystem functioning? Studies of are likely to be huge, given the very fragmentary the relationships between soil fauna diversity and knowledge we have regarding their , biology major ecosystem functions are particularly needed, and ecology, and their potential use in agriculture and especially at the landscape level. Functional classifi­ bioremediation. cation of soil animais may help us to estimate how functional redundancy is important in soil, and Acknowledgements whether species loss will have significant functional consequences to the ecosystem. The relationships We particularly wish to thank Diana Wall and Maur­ between biota above and below the soil interface, icio G. Paoletti for providing useful papers for this and how changes in one compartment may alter review, and Diego Bonilla (Insectos de Colombia) for the functioning of the other should also receive informations about commercialisation of Colombian more attention. "culonas". Thanks to two anonymous referees for • Which tools should be used to evaluate the eco­ reviewing this paper in details. nomic and social values ofspecies and biodiversity? How can we evaluate the importance of biodiversity for local to global markets? References • How can we identify "important" species on which we should concentrate our conservation efforts? 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