Interactions between Aboveground and Belowground Biodiversity in Terrestrial Ecosystems: Patterns, Mechanisms, and Feedbacks
Understanding linkages between the diversity of organisms above ground and that of organisms below ground constitutes an important challenge for our knowledge of how ecological communities and processes are determined at both local and regional scales. Furthering this understanding may render information critical to the conservation of species, ecosystems, and the services they provide to humanity. Because belowground diversity is often difficult to measure and many organisms are poorly understood or have yet to be described, discerning patterns of correlation among aboveground and belowground species, and the mechanisms causing these patterns, could provide a proxy for developing approaches for protecting belowground species. In addition, linkages between diversity above ground and below ground may be functionally important at the eco system scale in terms of the maintenance and stability of ecosystem processes and the persistence of keystone species or other species with strong ecosystem effects (Chapin et al. 1997, Groffman and Bohlen 1999, Wall and Moore 1999). These are immediate concerns applicable to issues of global change, including tradeoffs between development and ecological sustainability (Wolters et al. 2000). An international workshop convened in October 1998 under the auspices of the SCOPE (Scientific Committee on Problems of the Environment) Committee on Soil and Sediment Biodiversity and Ecosystem Functioning sought to address such questions about relationships between aboveground and belowground diversity. This article takes a two-step approach to evaluating these relationships. First we review the evidence for correlations between diversity of aboveground and belowground organisms, both on local and across larger biogeographical scales. If correlations exist, we ask whether they result from direct linkages among groups of organisms above and below the surface. Second, where cause-and-effect relationships are apparent, we synthesize what is known about the mechanisms involved in those relationships. Is high aboveground diversity, either collectively or for specific taxa, correlated with high belowground diversity? Where there are broadscale correlations of aboveground and belowground biodiversity, do these patterns hold at more local scales? For example, because the shape of trajectories for any one habitat or locality that lies within such broad patterns could vary substantially (Figure 1), can we predict the pattern of change in diversity above ground and below ground during natural and anthropogenically imposed disturbances? We review both data that support and data that oppose correlations between aboveground and belowground diversity; we then explore possible explanations for the patterns (or lack thereof). Correlation of aboveground and belowground diversity does not necessarily imply mechanistic linkages, but it is a first step in assessing whether such linkages exist. Before reviewing the data, however, we need to address several issues raised by the different scales of organisms and processes. The size of various organisms and their spheres of influence vary over several orders of magnitude, temporally and spatially (Beare et al. 1995) (Figure 2). For example, the processes influencing community composition both above ground and below ground might involve daily and other short-term fluctuations in abiotic conditions, seasonal fluctuations in phenology (Strong et al. 1984), yearly variations in climate, decadal or multicentury influences of succession, or geologic (more than a million years) evolutionary relationships (Ricklefs and Schluter 1993). Moreover, the various processes that link aboveground and belowground systems may operate at different scales of biodiversity, influencing, for example, genetic variation within and among populations, species richness and composition, diversity of functional groups, or ecosystem patterns at the landscape scale (Wolters 1997). Belowground, a species approach is not always practical, especially for microbial and many microinvertebrate taxa to which the traditional species concepts are difficult to apply. In such cases, taxanomic groups are commonly lumped into functional groups defined by their role in a community or ecosystem process (de Ruiter et al. 1994, Brussaard et al. 1997, Smith et al. 1997). These issues of scale—spatial, temporal, functional, and phylogenetic—can confound patterns of diversity and the inference of process from those patterns. Together they may negate any single, simple mechanism as the prime determinant of either aboveground or belowground diversity. Therefore, measurements and mechanisms involved in comparisons among taxa should be closely matched. Numbers of species above ground and below ground may be correlated when taxa in both realms respond similarly to the same or correlated environmental driving variables, especially across large gradients of disturbance, climate, soil conditions, or geographic area. In such cases, diversity in the two domains is not necessarily causally linked. Numerous examples illustrate that conversion of natural ecosystems to agriculture decreases both plant diversity aboveground and soil macrofaunal diversity belowground (Lavelle et al. 1994, Lavelle 1996, Wardle and Lavelle 1997). Coffee plantations exhibit a range of plant diversity, depending on management; as plantations are simplified aboveground, they show a significant decline in ant (Perfecto and Snelling 1995) and scarabaeid beetle (Nestel et al. 1993) diversity. Disturbance from land use change decreases species richness and abundance for plants, termites (Eggleton et al. 1997), and nematodes (Freckman and Ettema 1993, Wasilewska 1997). In relict arctic–alpine communities, diversity of endemic and relic plant species is positively correlated with high species richness of endemic soil fauna (Collembola, Acarina, Diplopoda, etc.). These plants and soil animal species persist together because of extreme microclimatic conditions (Rusek 2000). In other cases, as with soil microbes, simplifying the plant community leads to changes in microbial community composition or relative abundance despite little change in microbial diversity at the plot scale (Wardle et al. 1999b). Similarly, species diversity of different taxa may be correlated across different sites because of island biogeographic effects resulting from the size of suitable habitat fragments and their distance from sources of colonization. Such patterns could arise because of factors associated with a greater sampling area (that is, an increase in the number of individuals sampled, more habitat types, or larger population sizes), in addition to—or instead of—direct ecological interactions and high concentrations of species at certain sites (Rosenzweig 1995). The diversity of various taxa on different islands may also be influenced by island age, with older sites having greater species richness resulting from more time for both immigration and speciation (Borges and Brown 1999). The numbers of species above ground and below ground may be correlated also when direct ecological linkages exist, in which case the diversity is considered to be causally related. For example, aboveground diversity might promote belowground diversity—or vice versa—by increasing the variety of food resources (litter quality and composition), the range of environmental conditions (temperature, humidity), or the structural complexity of the habitat (Anderson 1994). High diversity in plant species can result in high diversity of litter quality or litter types entering the belowground subsystem. This resource heterogeneity can lead to a greater diversity of decomposers and detritivores (Anderson 1978, Tian et al. 1997, Sulkava and Huhta 1998) (Figure 3). Selective association of particular species with particular litter types has been shown for fungi (Widden 1986), Collembola (Klironomos et al. 1992), and millipedes (Dangerfield and Telford 1996). A survey of litter-feeding mollusks across forest types indicated a significant correlation between floristic diversity—and, presumably, diversity of carbon inputs—and mollusk diversity (Barker and Mayhill 1999). Root herbivore diversity can be related to the diversity of host plants (House 1989), and genetic diversity of the soil bacterium Burkholderia cepacia increases with increasing heterogeneity of organic substrates (McArthur et al. 1988). The “first link” hypothesis of Lavelle et al. (1995) proposes that plant diversity, because of production of diverse root exudates, can lead to diversity of soil the first link of a of effects resulting in diversity of other soil animal groups as heterogeneity may be related to plant diversity when the of important plant is to particular plant taxa, with for the diversity of aboveground (Strong et al. and belowground In other cases, however, belowground diversity is closely to the diversity of resource types, of plant species For example, a species of could result in greater resource heterogeneity than might several species of (Wardle et al. 1999b). In addition to to heterogeneity of food soil diversity can be related to diversity (Wardle and Lavelle 1997, Sulkava and Huhta Where plant litter to organic with this structural heterogeneity in the development of diverse communities (Anderson In comparisons of and litter in the and that certain in the in litter in the with other litter types, because of also that more diverse of litter in than in there may be a between the food and influences that aboveground litter has on the diversity of belowground of litter decreases the structural that it for use as and that diversity may diversity below ground and are a because the of many species above ground and the on such as plant species and structural diversity above which are often related to diversity of aboveground species et al. may have important for belowground diversity as A high diversity of resources and species in soil could to a high diversity above where certain species or functional groups are closely to groups below For example, et al. a correlation between the diversity of species and plant diversity, because different species of fungi different species of plants to different explanations for the patterns they (Wardle 1999). this pattern does not hold at the scale of functional types of communities can be associated with high diversity of plants, and high diversity communities can be associated with diversity of plants et al. 1995). communities also and these mechanisms could influence the diversity of aboveground communities, evidence for such is and that one of the species they in food in plant and functionally because other species of the same In addition, of specific belowground can a of effects the food that the of plant et al. et al. 1993). to such effects in soil food and and 1999). of the for these could be that many spheres of influence to ecosystem process and belowground species composition (Beare et al. 1995). these influences are the effects of and by and in the and in litter and organic and and soil as as direct many interactions among species are in the of effects on community composition to increase 1999). of correlation in diversity among particular groups of organisms can for several the species or groups could be to different abiotic or to the same abiotic but on different or scales. a regional scale different there is often an between and because termites to with quality or of organic and with of et al. 1994). broad gradients of abiotic conditions to diversity species in may be correlated between aboveground and belowground but taxa may diverse diversity is For example, et al. 1997, Lavelle et al. and and et al. 1995) diversity does not increase the plants and many other Second, species or groups could be interactions that diversity in the other that belowground species may be influenced by aboveground diversity because they are by within belowground food than by such as heterogeneity of from aboveground (Wardle and 1993, Ruiter et al. 1995). among and different can be and For example, can plant species richness in communities and Brown 1997). This in could aboveground diversity plant diversity aboveground herbivore diversity. root can a within the host plant that increases the of a the same host plant et al. 1993). Therefore, in to root the community of more and plant species richness and than in soil and Brown 1997). Similarly, effects of aboveground on the abundance of belowground organisms and of ecosystem as by root and litter can be either or The on the of the plant species and the environmental conditions under which it et al. These that not groups within either aboveground or belowground necessarily the same diversity when they are closely diversity in one could on the composition, than the diversity, of organisms in the other In in belowground diversity not aboveground diversity. Wardle et al. different functional groups of the and the composition of functional groups of belowground evidence for the of relationships between plant diversity and diversity of any of the belowground functional groups (Figure that soil is more to be related to the of the plant species to the quality of resource than to the diversity of the plant community These are to those in assessing the effects of plant composition and diversity on ecosystem processes and 1997). and evolutionary relationships can a large role in species diversity within communities (Ricklefs and Schluter 1993). These factors not necessarily aboveground and belowground taxa in a especially across in size and For example, for soil groups litter-feeding land the development of patterns (Barker and Mayhill diversity of these groups is not necessarily related to the composition of the plant effects of resource quality or may effects of resource The hypothesis a of belowground diversity at of resource of aboveground diversity and step in for a plants may belowground diversity of production than resources may a larger and more diverse soil and litter community and 1999). at the biogeographical patterns of richness in more closely to plant than to diversity (Eggleton 2000). the plot soil diversity correlation with plant diversity, but it show a correlation with aboveground plant across in the (Figure patterns may also hold for because of the of and in a but This mechanism more especially because it in plant communities, where often lead to and of plant diversity. comparisons of diversity in aboveground and belowground taxa are several for taxa among aboveground species have been Because of the mechanisms for aboveground species are to those for belowground species, these what patterns might when a variety of belowground taxa as have correlations in diversity among aboveground taxa, evidence for a that as an for the diversity of other taxa at the landscape plant diversity is correlated with greater diversity of aboveground in natural et al. and 1998) This pattern may have because are often (Strong et al. or because diversity positively to plant complexity et al. et al. the other with aboveground taxa in natural ecosystems depending on sampling and taxa of a of a ecosystem on the diversity of a aboveground to the diversity of aboveground of diversity for one are not necessarily for et al. 1993, et al. the other species across environmental or diversity, can patterns for taxa et al. 1993, and 1996, et al. Therefore, on changes in species composition of a across many different ecosystem types may of the regional diversity for many different This that a simple on diversity a habitat as has been may patterns of diversity that are important for conservation for belowground as as aboveground species. Where there are correlations among aboveground and belowground taxa, what are the ecological linkages by which aboveground belowground biodiversity, and vice species or functional groups above or below the to high on the other of the are of mechanisms by which organisms in one can in the is interactions An aboveground could be to a certain belowground for that of one of the such relationships within communities could to correlations in diversity aboveground and The is interactions The effects of a species or functional could influence or richness in the other The is richness in one diversity in the that richness is correlated between aboveground and belowground species and of species linkages and as as species or functional groups that provide a resource for species or functional These linkages where the association is both specific and for at one of the it need not be for both example, a belowground herbivore may on a certain species of but the plant is to have other and is not on any of The of can vary for or such as have a host many plant species and in the have such host that of the plant species, or a change in the of the plant species, could the of the and fungi exhibit a of variation in their host many have broad host are to a of plants et al. et al. 1995). the other the species of fungi that are is host specific In both and a plant may be by more than one species of The to which are can vary for in the of host between and their might lead one to that the are on the this is not The and related as in with a with can for in the of the their numbers to when a is and the other for the plant can on the of the For this the of certain or is more than species because the for and can be among and 1996). species and and belowground taxa can be closely but the does not necessarily lead to correlations of diversity. species or functional groups can have a large influence on composition, or diversity in the other necessarily diverse are a plant communities are often associated with or their immediate and may in a from to and as and 1996). of termites can soil organic carbon and plant and the floristic of and In the the of the and of plants as as landscape (Dangerfield et al. et al. the community in any need not be diverse to these effects on plant composition and diversity. mechanisms could lead to either or diversity, depending on the ecological effects of species above ground may influence conditions of below ground (or vice the effects on diversity could vary et al. 1997). Such mechanisms could increase diversity for example, they increase habitat heterogeneity or by species. species effects on community or ecosystem are large relative to their their influence by such mechanisms et al. 1996). the that those soil that are ecosystem plant by increasing of on plant community are et al. 1996, Lavelle et al. 1997, et al. 1999). in of the between and plant diversity, explanations predict that these effects could either increase or plant diversity, depending on et al. 1997, and Brown et al. 1999). Similarly, interactions in the can increase and of and these for plants 1994, 1994). by can the of plant plant et al. 1994). of these interactions influence conditions and of conditions for organisms on the other of the soil is not necessarily with increasing their diversity. mechanisms by which effects could diversity are keystone species, direct and environmental there may be in which one particular species the role in community diversity a in and in other cases, several species could have the same as when effects are by the abiotic Where keystone species the abundance of species by or they can greater diversity among species et al. 1996). The to which this mechanism between aboveground and belowground communities is but there is strong for keystone effects across the soil For example, belowground can or aboveground in effects on plant The of plant by nematodes can be to greater than that by in soil are also specific in their If this belowground by species, it could increase plant diversity. Similarly, by aboveground could diversity of belowground interactions when a species or functional in one the persistence of many species in the the functional can promote plant diversity of by increasing of species et al. et al. The environmental conditions that they persistence of a greater diversity of organisms in the other an and litter have a critical on and relative humidity), et al. Tian et al. 1993, Lavelle et al. 1997), it can be difficult to between and and by large can change soil and and the that these increase environmental they increase diversity of belowground organisms as and 1997), this to be Similarly, belowground organisms can the for aboveground species. In and are ecosystem that may have important aboveground these organisms they organic and to that influence soil and soil processes such as carbon carbon in of organic and other processes that are important of plant and et al. 1994, et al. 1995). These and lead to to which plant are or in which may to aboveground diversity Soil by can also influence plant composition and diversity and 1994, and other with in the soil be as aboveground or belowground In cases, the of certain species or functional groups could lead to diversity in the other the of leads to diversity in litter in ecosystems (Rusek with the have a on soil and as a result of resource quality (Wardle et al. species can also abundance and diversity of of the The of mechanism for correlations in diversity are those in which greater diversity in one leads to greater diversity in the A for this is that a diversity of carbon from aboveground lead to a greater variety of food resources for belowground more diverse soil communities greater (Figure 3). diversity may influence aboveground diversity as example, in interactions between and plants et al. in diversity of aboveground and belowground taxa on both the of the interactions among and the and scales of the ecological factors influencing the of the organisms is the evidence for correlation between aboveground and belowground diversity is broad gradients in or environmental conditions, aboveground and belowground diversity may but the relationships are often more at more local scales. Where correlations exist, they are not always in Second, there are a variety of mechanisms by which organisms above ground could community composition and diversity below and vice not of these mechanisms necessarily lead to correlations of species richness in the two domains (Figure A in comparisons is the lack of information on soil have a knowledge of aboveground than belowground organisms, yet a large of global diversity below as as of soil and species are and 2000). comparisons are for these functional groups are often for soil microbial and the other the of species for the diversity of aboveground organisms and soil and which have been more and This in comparisons of aboveground and belowground diversity. of that both aboveground and belowground biodiversity, as as their effects on ecosystem processes and community should be a strong et al. 1997, Wall et al. 1997, Wall and Moore 1999). Understanding patterns of diversity is a of because of the of natural ecosystems or not we strong correlations among aboveground and belowground diversity, the to the between these two domains our understanding of the mechanisms that shape ecological communities, and our to The the SCOPE Committee on Soil and Sediment Biodiversity and Ecosystem an and the of and the The for to host the workshop between and Biodiversity and for Ecosystem and in The This the of the SCOPE Soil and Sediment Biodiversity and Ecosystem Functioning and on of the relationships between aboveground and belowground diversity at local and regional scales. A correlation between aboveground and belowground diversity across broadscale of climate, and an of many correlation increase step or or correlations despite broadscale correlations A understanding of the mechanisms at both local and regional scales is to of diversity and conservation of influence for aboveground and belowground diversity. The scales of organisms and interactions aboveground and belowground diversity vary over several orders of magnitude, as do gradients in in and resources among aboveground and belowground taxa may lead to correlation between aboveground and belowground diversity at the local scale than there is across broad patterns of diversity above ground and below it is to both and of and forest with of from 1996, Soil with of as from in the hypothesis that heterogeneity of carbon substrates from aboveground organisms positively influence belowground diversity. This mechanism strong of diversity in belowground it should be in the of other and of leads to diversity of The critical link in this step is how diversity resource in ecosystems where aboveground provide large of high quality food for decomposers and 1994, and Groffman plants aboveground carbon could also effects on the composition and diversity of plant The between diversity and resource diversity on several functional of the species including composition of and organisms, their in in Brown and 1989), and their in time et al. 1997). resource heterogeneity leads to diversity of and The critical link is the of the can vary We that the of of detritivores is with species either high or the show an of food Such a may not hold for other (Strong et al. and plant which to be more A of a of to species of or belowground diversity be to increase with number of substrates et al. 1988). step resource than leads to diversity of The critical link is the of resource quality to the hypothesis 1978, If diversity is at of environmental then at of resource quality the diversity of detritivores and decomposers be in any of a species can use the at high a species are to the of the hypothesis in this is evidence for it at the scale of a for diversity is that information on species richness in ecosystems is of detritivores or belowground leads to diversity of organisms at in belowground food The critical link is If are than in belowground food patterns of in belowground food may effects of resource heterogeneity and Ruiter et al. 1995). could arise from by aboveground because aboveground and belowground food can be in of a belowground food correlations among diversity of various groups of different plant functional correlations are and not significant because diversity of belowground taxa more to changes in plant functional composition than to changes in plant The correlation with a is significant at from Wardle et al. with from the of between soil diversity, plant diversity, and plant in at of different with different of by and of forest species. A the between species richness of plants and species richness of soil the as the number of the is not the between aboveground plant and species richness of soil both are significant but the correlation is with species of the forest than with richness including species. with from A whether of aboveground and belowground taxa be that lead to correlation are at as as those that lead to interactions direct or other community interactions or effects on environmental that influence species in the other scale to the over which of species within the groups scale to the time scales over which species within the groups respond to conditions