Some Representative Subterranean Communities

Among shallow subterranean habitats, representative communities of hypotelminorheic (Lower Potomac seeps, Washington, DC), epikarst (Postojna–Planina Cave System, Slovenia), milieu souterrain superficiel (MSS) (central Pyrenees, France), soil (central Pyrenees, France), calcrete aquifers (Pilbara, Western Australia), lava tubes (Tenerife, Spain and Lava Beds National Monument, California), fluvial aquifers (Lobau wetlands, Austria), and iron-ore caves (Brazil) are described. Among non-cave deeper habitats, communities of phreatic aquifers (Edwards Aquifer, Texas), and deep phreatic aquifers (basalt aquifers, Washington) are described. Among cave habitats, representative tropical terrestrial (Gua Salukkan Kallang, Sulawesi, Indonesia), temperate terrestrial (Mammoth Cave, Kentucky), chemoautotrophic (Peştera Movile, Romania), hygropetric (Vjetrenica, Bosnia & Herzegovina), anchialine (Šipun, Croatia), cave streams (West Virginia and U.K.) and springs (Las Hountas, Baget basin, France) communities are discussed.

Geography of Subterranean Biodiversity

Globally, for troglobionts, southern Europe, especially the Dinaric karst, and the Canary Islands are regions of high richness. For stygobionts, southern Europe, especially the Dinaric karst, is a hotspot. Other sites are typically chemoautotrophic and/or phreatic. In Europe and North America, there appears to be a ridge of high troglobiotic and stygobiotic diversity in southern Europe and the southeast United States that corresponds to an area of long-term high surface productivity. In Europe, local diversity is a small component of regional stygobiotic diversity and the importance of spatial heterogeneity, historical climate stability, and productivity are both scale and spatially dependent. Habitat availability seems especially important at smaller scales. The analogy with islands in ecological time is most appropriate at scales smaller than caves, such as seeps or epikarst drips, and the analogy with caves in evolutionary time is more appropriate at larger scales, such as karst basins or contiguous karst areas.

Colonization and Speciation in Subterranean Environments

Colonization and speciation in subterranean environments can be conveniently divided into four stages. The first step is colonization of subsurface environments. There is a constant flux of colonists into most subterranean habitats. The second step is the success (or failure) of these colonizations. The third step is speciation. Under the Climate Relict Hypothesis (CRH) surface populations go extinct but under the Adaptive Shift Hypothesis (ASH) they do not necessarily do so, and speciation can be parapatric. There is strong evidence for the CRH among temperate zone fauna, and growing evidence for the ASH in tropical caves, especially lava tubes. The final step is possible further speciation as a result of subsurface dispersal. Detailed analysis of the evolutionary history of the isopod A. aquaticus in the Dinaric karst, diving beetles Paroster in a calcrete aquifer in Western Australia, and trogloxenic Leopoldamys neilli in Thailand reveal some of the complexities of species’ phylogeography.

Biotic Interactions and Community Structure

A general pattern emerges from studies of subterranean communities. At a regional scale, hydrogeological and historical factors exert a controlling influence on many species, and the importance of species interactions is small. This is the pattern of the Jura Mountain groundwater communities. At a smaller geographical scale, there is little variation in hydrogeological or historical factors. For example, in both the Slovenian epikarst and Lyon aquifer studies, there was little if any variation in hydrogeological or historical factors. Species did differ in their occurrence along physicochemical axes, and these differences may well be the result of competition. Finally, some intensively studied communities show high levels of competition and predation, so strong that divergence rather than convergence occurs. There remains a gap between these somewhat unusual species combinations (beetles and cricket eggs, Appalachian cave stream invertebrates, Dinaric Niphargus, Australian calcrete diving beetles) and the broader scale community studies.

Conservation and Protection of Subterranean Habitats

A critical factor of the subterranean fauna and one that increases the risk of extinction is geographical rarity. Some stygobionts and troglobionts are also numerically rare. Subterranean organisms are also at increased risk of extinction because of low reproductive rates, and in the case of bats, because of their propensity to cluster in large numbers in a few caves. Threats to the subterranean fauna are of four general kinds—alteration of the physical habitat, changes in water quality and quantity, direct changes to the subterranean fauna, and global warming. The selection of sites for preservation requires detailed inventory data, but available evidence suggests that a majority of species can be protected at least at one site and that a relatively small percentage of total land area is required. A variety of mechanisms are available for site protection, including listing as a Ramsar wetland and as a UNESCO world heritage site.

Adaptations to Subterranean Life

The loss of characters, especially eyes and pigment, in subterranean animals has attracted the attention of biologists since their first discovery centuries ago. Adaptationist ideas with regard to subterranean organisms were originally developed, not in connection with loss of eyes and pigment, but rather in connection with constructive changes such as appendage elongation and elaboration of extra-optic sensory structures. Three studies of adaptation epitomize adaptation as it applies to subterranean species. In Poulson’s study of life history and metabolic and neurological changes in cave fish, his basic approach was comparative, using related surface-dwelling species. Using quantitative genetics, Culver and colleagues studied the amphipod G. minus, focusing on the adaptation to the darkness of caves. Jeffery and colleagues focused on the causes of eye and pigment degeneration in the Mexican cavefish A. mexicanus. Using an array of techniques, they demonstrated the critical role pleiotropic selection plays.

Survey of Subterranean Life

A wide variety of organisms are found in subterranean habitats and they have varying degrees of dependence and permanence in these habitats. Some species, stygobionts and troglobionts, have an obligate dependence on subterranean habitats, and are found nowhere else. Other species have an obligate dependence on caves and other subterranean habitats, such as bats and aquatic insects, but only spend part of their life cycle in caves (stygoxenes and trogloxenes). Others can spend their life cycle in or out of caves (stygophiles and troglophiles). There are 21 invertebrate orders that have over 50 stygobiotic and troglobiotic species. Among vertebrates, salamanders and especially fishes are also well represented in caves and deep aquifers. Although the information obtained is very informative, very few subterranean species have been maintained successfully in the laboratory. There are a few specialized collecting techniques that are very useful, especially in non-cave subterranean habitats.

Sources of Energy in Subterranean Environments

Although subterranean habitats in general and caves in particular are often held to be extremely energy-poor (oligotrophic) environments, not all are. Compared to surface habitats, subterranean habitats are nutrient-poor, especially because there is no photo-autotrophic production and chemoautotrophy appears to be uncommon. On the other hand, these differences are not always pronounced. For example, the quantities of carbon fluxes in cave streams are in the range of those reported from surface streams. In some subterranean systems, chemoautotrophy is the main source of energy, but more typically subterranean communities depend on allochthonous sources of organic carbon. The major source of carbon in interstitial habitats is Dissolved Organic Matter (DOM) from surface waters. The major sources of carbon for cave communities are (1) water percolating from the surface, (2) sinking streams that enter caves, and (3) activities of animals moving in and out of caves.

The Subterranean Domain

The main subterranean habitats are: small cavities—interstitial spaces beneath surface waters; large cavities—caves; and shallow subterranean habitats—voids of various sizes close to the surface. The defining feature of all these habitats is the absence of light. Environmental variation is also reduced and most subterranean habitats rely on nutrients transported from the surface. The aquatic component of caves includes water percolating from the surface (including epikarst), streams, and resurgences. Terrestrial habitats include epikarst, and the vadose zone. The aquatic interstitial habitat is comprised of the water-filled spaces between grains of unconsolidated sediments. Shallow subterranean habitats are ones close to the surface. They include the hypotelminorheic, interstitial, epikarst, MSS, soil, lava tubes, calcrete aquifers, and iron-ore caves. They share an absence of light, close surface connections, relatively high nutrient levels relative to other subterranean habitats, and the presence of species highly modified for subterranean life.

Ecosystem Function

An important aspect of all aquatic subterranean ecosystems is the nature and connectivity of surface inputs. A theme common to both is heterogeneity of inputs that exist at even the smallest scale. At least in cave streams, carbon appears to be limiting. Studies at the scale of entire caves are of two very different kinds. For caves with surface inputs, inputs from percolation water are quantitatively less important than inputs from sinking streams, but are qualitatively more important because they occur throughout the cave and form the basis for the biofilm. Sulfur-oxidizing bacteria are the trophic base for most chemoautotrophic cave communities. Only two ecosystem studies of an entire karst basin have been carried out. For the Dorvan basin in France, most carbon entering the ecosystem is DOC, and there is considerable storage of organic carbon in sediments. In the Edwards Aquifer of Texas, chemolithoautotrophy contributes to all the components.