TREE vol. 15, no. 6 June 2000 0169-5347/00/$ – see front matter © 2000 Elsevier Science Ltd. All rights reserved. PII: S0169-5347(00)01868-1 2 2 3
D
uring the past years, importantstud-ies have been carried out not only to quantify the species richness of ani-mals at regional or even worldwide scales, but also to explain the causes of species richness within various earth zones. Prominent examples are the huge biodiversity of invertebrates living in the rain forests and the deep sea. The groundwater domain forms an unseen ‘ocean’ beneath our feet, which is docu-mented to extend to a depth of several kilometres, with an enormous historical and spatial continuity. Global documen-tation of the diversity of groundwater animals (i.e. the study of all animal groups for which enough available in-formation exists) at continental or world-wide scales is scant1,2. Moreover, our knowledge of the underlying causes for the observed species richness over large groundwater areas is also limited. Two publications by Sket3,4now redress this deficiency, based on detailed quanti-tative analysis of the species richness of animals living exclusively in subsur-face waters (they are called hypogeans or stygobites).
Interest in these studies can be in-creased if the subsurface hydrosphere and its organisms are seen as a complex system5. Just below the surface, the up-per sedimentary layers (extending down to a few metres), which remain in direct contact with an aquatic or an aerial and/ or terrestrial system, form a dynamic, energetically rich source–sink zone. This zone is frequently colonized by aquatic surface (epigean) organisms as well as by stygobites. With increasing distance from the surface water or terrestrial habi-tats (up to several hundred metres lat-erally or vertically), the groundwater be-comes more oligotrophic and poorer in oxygen. Consequently, epigean species vanish and stygobitic species prevail. Even deeper groundwater layers consti-tute an extreme environment charac-terized by extended oligotrophic and hypoxic (or even anoxic) conditions. This zone is colonized by many specialized microorganisms, including both Bacteria and Archaea6. Because the groundwater domain is sometimes perceived as an ‘extreme environment’ where only highly adapted animals live, the idea of low biodiversity has intuitive appeal7. Sket’s synthesis3,4offers useful information on this topic.
Species richness of groundwater animals
For one large group of Crustacea, the Malacostraca, Sket3 was able to compare hypogean (stygobitic) and epigean species numbers. Some 2130 malacostra-can stygobitic species were recorded worldwide; however, the total worldwide epigean marine and freshwater malaco-stracan fauna amounted to approxi-mately 20 500 species. On a continental scale, Sket3,4showed that in Europe by 1998, approximately 2400 stygobitic spe-cies were recorded in this continental groundwater domain, but this figure is actually estimated to be 3000. These numbers are low compared with the epigean surface freshwater-dwelling fauna, which in Europe is estimated to be approximately 12 500 species. However, the idea of an impoverished groundwater fauna has to be accepted cautiously, be-cause there are cases where biodiversity isn’t as low as it appears7.
Indeed, it appears that the aquatic stygobitic fauna is quite unique, com-pared with the fauna of surface waters, owing to the dominance of crustacean species (e.g. in Europe stygobitic species account for approximately 40% of the total crustacean fauna) and the virtual absence of Insecta (representing about 50% of the total European animal species living in surface waters). However, at a global scale, several major groups of Crustacea are exclusively represented by species living only in subsurface waters (e.g. the Remipedia, Thermosbaenacea and Spelaeogriphacea). The species rich-ness of several other crustacean groups (Copepoda, Cyclopoida, Harpacticoida, Syncarida, Amphipoda, Isopoda and partly the Ostracoda) in groundwater attain values closer, or even higher, than those recorded at comparable scales in sur-face freshwater habitats3,4. It is also well known that there is a large number of sty-gobitic relict species belonging to once widely distributed surface-dwelling ani-mal groups, which became extinct in their original surface–water environment dur-ing the earth’s history. Thus, many repre-sentatives of the groundwater fauna are especially suited for studies dealing with evolutionary–ecological topics.
The number of endemic stygobitic species examined at regional scales is apparently higher in karstic systems than in porous sediments of alluvial aqui-fers. This could be a result of the greater
isolation of karstic systems compared with ecosystems developed in porous allu-vial sediments. For instance, at the conti-nental scale the Dinaric Karst region, espe-cially in Slovenia3,4, forms a hotspot diversity area with the highest rate of endemic stygobitic species (about 80% of the total stygobitic fauna of the Dinaric Karst). Culver and Sket8, and Wilkens et al.9 provide additional information on hotspot areas of groundwater biodiversity. Identifi-cation of these sites is important not only for their intrinsic scientific interest (e.g. it prompts a closer investigation of the causes that produce the high species rich-ness observed in such areas), but also because it promotes the implementation of adequate environmental protection measures for these parts of the Earth.
Causes leading to high stygobitic diversities
The high biodiversities documented at a regional scale, which are well represented by the crustacean fauna, require explan-ation. Sket3,4enunciates several causes for the high diversities of stygobitic fauna in the Dinaric Karst area, which could act either synchronously or independently: (1) the lack of abundant and/or strong competitors and predators, such as in-sects in the subsurface hydroscape; (2) a high propensity for speciation through either microgeographical (see above) or ecological isolation (i.e. a high level of par-titioning of the subterranean space and a high ecological specialization) of various stygobitic species, which is visible in sev-eral crustacean groups; (3) favourable thermal environmental conditions at a regional level; and (4) a dynamic local palaeogeography, which has caused nu-merous spatial changes at the earth’s sur-face and within the subterranean hydro-scape since the Tertiary period. During this period, the repeated active coloniz-ation by surface marine and/or freshwater animals, which already display the abil-ity to speciate and adapt to new local environments in conjunction with low rates of extinction in a more thermally sta-ble subterranean environment, lead to an increase in the number of stygobitic spe-cies throughout the whole of the Dinaric Karst. Several crustacean groups, such as the Asellidae isopods, the amphipods of the genus Niphargus, the ostracod Candoninae, and the cyclopoids belonging to the gen-era Diacyclopsand Acanthocyclops(which produced many stygobitic species in Europe), are well known for their evo-lutionary flexibility3,4. Such animals are morphologically variable, prone to spe-ciation and can easily adapt to local en-vironments. In Sket’s study pertaining to various stygobitic lineages, this process already begins at the Earth’s surface.
NEWS & COMMENT
NEWS & COMMENT
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Martens and Schön10 show that in freshwater-dwelling Ostracoda there are two groups that display high evolutionary plasticity, the cypridids and the can-donids. The cypridids, with well de-veloped ocular structures and natatory capacities, diversify minimally within the groundwaters; however, the surface-dwelling candonids have unpigmented ocular structures, are devoid of swimming setae and are predisposed to colonize the subsurface aquatic environment. Thus, the Candoninae became the most species rich stygobitic group belonging to the Ostracoda1. The evolutionary model of the repeated active colonization of the subterranean environment by epigean organisms, was proposed by Sket3,4 in the 1960s, and has subsequently been used by various scientists11,12. In our opinion, this model offers the most compelling explan-ation for cases of highly diverse subter-ranean aquatic faunas known to occur in Europe at a large (regional) scale (e.g. around the Mediterranean basin1,2).
Prospects for groundwater ecology
Groundwater ecology seems to have entered into a new phase of development where the topic of biodiversity in subsur-face waters has taken a new dimension. With the refinement of microscopic ob-servations of animal morphology, and also with the techniques used in molecu-lar and phylogenetical systematics, we expect to see a substantial rise in the recorded number of hypogean species. At closer morphological and/or molecu-lar analysis, widely geographically dis-tributed stygobitic species turn out to represent complexes of cryptic species13,14. We consider that besides pursuing the identification of species richness in ground-water, we should continue to subtly ob-serve the diversity of adaptive solutions of stygobites.
A recent contribution by Claret et al.15 makes exactly this point, stressing the necessity for more autecological studies on subterranean-dwelling animals. This would allow us to understand better the extent of the adaptive radiation process in groundwater for various animal groups, compared with well documented cases (e.g. those on ostracods, copepods and amphipods) in old and deep lakes10. It would be especially useful to evaluate the real extent of the diversity and dis-parity of stygobitic lineages living in karstic systems, compared with related animal groups specialized to interstitial life in sand and gravel substrata. It would also be interesting to know if hotspot areas are always linked to regions ex-posed to numerous climatic or geological changes, as argued by Sket3,4.
One of the major attractions of fur-ther large-scale studies on groundwater biodiversity lies in its potential capacity to decode the evolutionary history avail-able in many stygobitic lineages, which have been preserved underground dur-ing various geologic epochs. Excellent examples have been provided by stygo-bitic crustacean groups, such as the Syncarida, Ostracoda or Remipedia2,9.
Acknowledgements
We thank Boris Sket, David C. Culver, Janine Gibert, Pierre Marmonier, Andrew Boulton, Koen Martens, Guiseppe Messana, Janet Reid and Fabio Stoch for productive discussions on this topic, and the Austrian foundation FWF (Vienna) for financial support to the project P-11149 BIO awarded to D.L.D.
Dan L. Danielopol Peter Pospisil
Institute of Limnology, Austrian Academy of Sciences, A-5310 Mondsee, Austria (dan.danielopol@oeaw.ac.at; peter.pospisil@netway.at)
Raymond Rouch
14, rue du 19 mars 1962, F-31620 Fronton, France
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4 Sket, B. (1999) High biodiversity in hypogean waters and its endangerment – the situation in Slovenia, the Dinaric Karst and Europe. Crustaceana 72, 767–780
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11 Rouch, R. and Danielopol, D.L. (1987) L’origine de la faune aquatique souterraine, entre le paradigme du refuge et le modèle de la colonization active. Stygologia 3, 345–372
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species of the Diacyclops languidoides-group (Copepoda, Cyclopoida) from groundwaters of Austria. Hydrobiologia 412, 165–176
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