Biodiversity in ground waters

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Biodiversityin Ground Waters Pierre Marmonier, Marie-Jos6

Philippe Vervier, Janine

Dole-Olivier

Despite the importance of ground waters in the global water cycle, their ecology and biodiversity have only recently received attention. Three areas are currently 6eing

studied: (I) the origin and colonizationof ground waters, (2) the adaptation of animals to the subterranean environment, and (3) the role of ecotone between surface and ground waters. There are still several gaps in our knowledge of groundwater biodiversity (at the genetic level, the species level, the functional group level and the ecosystem level) to which future research

must 6e directed. Underground waters are the largest hydrological unit after the world’s oceans, representing 97% of all global freshwaters’. Groundwater is present in three main kinds of aquifer: karstic (limestone), fissured (granitic) and porous (alluvium) see Box I. Although they are exploited for drinking water, agriculture and industry, ground waters are amongst the most poorly known ecosystems2m3. Generally speaking, subterranean waters have been studied mainly by hydrogeologists, hydraulics engineers and hydrochemists; however, the management of this vast resource also requires consideration of the fauna within the ecosystem. Classically, ground waters have been considered as having less habitat diversity than surface water environments, this seeming poverty being characterized by reduced physical and chemical variability and the apparent lack of primary production4. For example, a porous aquifer may be considered as a rather homogeneous interstitial habitat; the seasonal cycles that have so much influence on the surface water environment have a much reduced inPierre Marmonier fondamentale

is at the Laboratoire

et appliquke,

BP 1104, 7101 I Chambery, is at the Centre ouvelables,

31055 Toulouse

versitk

Souterraines,

fluence on subterranean ecosystems. However, recent investigations have highlighted the local and regional heterogeneity of aquifers, and have considered the groundwater environment as a landscape5f6. Original interest in subterranean fauna was in the description of ‘living fossils’ with strange body shape4. In fact, ground waters harbour all the major invertebrate groups4, the assemblages being composed of both narrowly specialized hypogean (subsurface) and generalist epigean fauna (surface) - see Box 2. For most of these invertebrate groups, abundance and biodiversity at local scales are IOWANS. These organisms function actively within the subterranean ecosystem as an ‘anticlogging’ process9; combined with various physical and chemical mechanisms, the groundwater fauna are involved in bank filtration processes (filter effect) such as the transformation of organic matter (observed in many other systemslO). Because the groundwater foodwebs are short and the energy sources are weakly diversified, groundwater fauna and its biodiversity seem to be highly

sensitive to environmental changes and could be considered as the most efficient tool to understand the func-tioning of the subterranean ecosystem. Therefore, the biodiversity of ground waters needs as much attention as has been recently directed towards surface environments. Recent developmentsand debates

The colonization of the groundwater environment by organisms occurred from both marine and freshwater ancestors, and this has led to the proposal of two alternative models: the ‘refugium model”’ and the ‘active colonization model’12. During the 1950s and 1960s subterranean waters were considered as a refuge for surface animals to avoid the environmental constraints of surface water environments (such as climatic variations). Botosaneanu and Holsinger ” focussed on the importance of preadaptation of the ancestral organisms, which found subterranean conditions not entirely different from those of their previous habitat. This ‘refugium model’ could account for the occurrence of rare organisms in very limited areas and the existence in a given lineage of only those few genera that have evolved species adapted to groundwater environments.

d’Ecologie de Savoie, Vervier

des Ressources 29 rue Jeanne

RenMarvig,

France; fanine Gibert

and

are at Hydrobiologie

et

U.R.A. CNRS no 1451, Uni-

Lyon I, 43 Bd du

Villeurbanne,

392

Cedex,

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Universite

France; Philippe

d’Ecologie

CERR-CNRS,

Marie-Jo& Ecologic

Gibert and

I I Novembre

1918, 69622

France 0 1993. Elsevier

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In contrast, Rouch and Danielopoll2 focussed on the active colonization process, suggesting that the settlement of fauna in ground waters is better explained by the progressive extension of the species’ original distribution linked to their exploration capacities and their ecological tolerance. Following Rouch and Danielopol”, preadapted, and especially generalist, species colonized ground waters during ‘stable’ periods without the pressure of any environmental constraints using the various transitional zones (ecotones) between surface and groundwater environments. This active colonization continues to take place; it can be observed in the rapid colonization of subterranean environments created de nova in volcanic islandst3. The ‘active colonization model’ thus provides a single scenario for the settlement of animals in ground waters rather than a series of circumstantial explanations. As a result of the debate centred around these two perspectives, the

perceived status of epigean organisms and groundwater biodiversity has changed. Previously considered as ‘foreign elements’ in subterranean waters, surface animals are now seen as an active component of the system. In the same way, groundwater biodiversity is now considered as a dynamic characteristic of the system. It can vary over time and not only during climatic crises. The most striking feature of groundwater organisms is that they look alike’4p15: most of their morphological characteristics (Box 2) are evolutionary regressions, and apparent acquisitions of new features are rare. According to Romeror6, this is a case of convergent evolution. This ‘selectionist’ point of view underestimates other evolutionary mechanisms such as neutral mutations, pleiotropy, or developmental constraints. From studies of amblyopsid fish, Poulsont7 proposed a hypothesis of accumulated selectively neutral mutations. For crustaceans, Culver and Fong15

suggested the hypothesis of structural reductions, which requires the existence of negatively pleiotropic genes for both reduced eye size and increased antenna development. Tested on the amphipod Cammarus minus, this later hypothesis involves energy economy in embryo development’8, which has yet to be clearly demonstratedig. Jones and Culver2o proposed that a reduction of unused visual sensory structure could lead to functional improvements in other sensory systems, by decreasing the amount of noise’ and increasing the relative amount of the central nervous system used for nonvisual sensory perception. Similarly, a reduction in body size can be a consequence of the animal’s paedomorphic development”. These morphological specializations to life in the interstices represent examples of ‘exaptation”2, which are characters evolved for other uses for for no function at all), and later seconded (or ‘co-opted’) for their current role.

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Despite the morphological convergence, groundwater organisms are not a homogeneous group. Recent developments in the study of their physiology highlight the diversity of responses to an environmental constraint. For example, groundwater fauna present a variety of different strategies to cope with oxygen deficiency23; thus, a weak morphological diversity can mask a high diversity of potential physiological reponses. The transition zone (or ecotone) between surface and ground waters plays an important role in the recovery of surface water assemblages after a disturbance. For example, the interstitial habitat of river sediments can provide a potential ‘refuge’ or ‘storage’ zone for epigean fauna during floods, a phenomenon that is the subject of current field and laboratory experiments24c25. The species richness of such ecotones is generally higher than in deep ground water because of the oxygen and organic matter exchanges with surface systems. Epigean fauna, the true ecotone dwellers, and deep groundwater organisms are found together in these contact zones. Thus, the species richness of the ecotone is generally intermediate between the high diversity of the surface environment and the low diversity of deep ground waters, hence the ‘edge effect’ is rarely observed in such ecotone8.

Major gaps and further studies The biodiversity of ground waters can be considered at four major levels. First, at the genetic level, geographic isolation of populations (generally confined in areas of reduced size) has been documented in terrestrial cave fauna26r27.Further research on groundwater fauna must therefore focus on gene flow and population limits. In the subterranean environment, the spatial frag mentation of populations ranges from weak isolation in large floodplains, where a clear hydric continuum can be observed in the ground waters, to the extreme isolation characteristic of populations inhabiting karstic systems. Secondly, at the species level, human disturbances as well as long term climatic and environmental changes govern biodiversity. To detect changes in biodiversity, we need both series of observations and comparisons between many sites. Thus, it would be important to define the ‘potential biodiversity’ for any given groundwater system, corresponding to the potential number of species that can be harboured by that system within its environmental and historical context. The potential biodiversity can vary considerably from one watershed to another (see Box 3) and for many regions (arctic, tropical and equatorial) is still poorly known28,29.

1993

Thirdly, biodiversity integrates not only the number of species but also their functional role. Therefore, for groundwater systems, including the adjacent ecotones, one must differentiate between functional groups, i.e. groups of species with similar effects on ecosystem function30*3’. However, because most groundwater organisms have very close feeding strategies, i.e. mostly detritivores and carnivores-detritivores4, the differences between other ecological requirements have been recently highlighted3*. These functional groups are thus defined according to their reproduction strategies, nutritional requirements, dispersal ability, and their sensitivity to disturbances. Within this context, the ecological redundancy between species (sense Walker3?) is very low in each functional group. Therefore, groundwater fauna need a higher priority in conservation efforts34. Finally, at the ecosystem level, the role of groundwater fauna in nutrient cycling is still poorly documented. The action of subterranean fauna on the physical characteristics of the groundwater environment (e.g. porosity) and the transformation of the organic matter require attention. One would expect that the efficiency of this action will be related to biodiversity, a basic characteristic of the assemblage. In conclusion, groundwater fauna are amongst the least studied group of organisms, but also potentially the least disturbed by human activities. The world’s groundwater systems are one of the last and most immense environmental units, approaching pristine in some locations. This vast system is of crucial importance both in the function of surface ecosystems and for human survival. Ground waters already represent a major part of drinking water for many countries and this exploitation is expected to increase. Therefore, in future the structure, function, and biodiversity of groundwater environments must be integrated into general ecology and environmental studies. Acknowledgements We thank G.H. Copp (University of Hertfordshire, UK) for editing the english text.

References 1 UNESCO ( 1986) Pollution et Protection des Aqoifkres, UNESCO

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2 Danielopol. D.L ( 1982) PO/. Arch. Hydrobiol 29, 375-386 3 Cibert. 1. Am. WaterRes. Assoc. (in press) 4 Ginet, R. and Decou, V. (1977) Initiation 2 la Biologie et 2 I’Ecologie Souterraines, Delarge 5 Rouch, R (I 986) Stygologia 2, 352-398 b Ward, J.V. 11989) / N. Am. Benth. Sot. 8, 2-8 7 Pennak, R. and Ward, 1. (1986) Arch Hydrobiol. Suppl 74, 356-196 8 Gibert, J., Dole-Olivier, M.J., Marmonier, P. and Vervier, P l I9901 in The Ecology and Management of Aquatic-Terrestrial Ecotones (Naiman, R.J. and D&s, H.. eds), pp. 199-225. Parthenon Publishing Group 9 Danielopol, D.L. (1984) Verh. lnternat. Verein. Limnoi. 22, 1755-l 761 IO Tietjen J.H. (19801 Microbiology35. 335-338 I1 Botosaneanu, L. and Holsinger, J.R. I I99 I ) Stygologia 6, I I-39 12 Rouch, R. and Danielopol, D L. (1987)

Numerous studies have 6een published on the skewed 6irth sex ratios among nonhuman primate populations. Sometimes the obsewed tendencies in sex ratio variations have been contradictory, and their adaptive significance has been controversial. Recent studies seem to reveal that the local resource competition among philopatric sex is the most important selective force affecting primate birth sex ratios. However, our understanding on this issue is still greatly hampered by the lack of exact knowledge on male reproductive success and the proximate mechanisms to vary sex ratios. Sex ratio variation has been a controversial topic’s2. Fisher’ proposed that the total parental expenditure incurred in respect of offspring of each sex should be equal and that the sex ratio would therefore adjust itself. Under what conditions should parents vary the sex ratios of their offspring? And is there evidence that they actually do so? Among diploid organisms such as mammals, in which the sex is determined chromosomally, observed sex ratio variations are usually slight, if ever detected’. However, since Trivers and Willard4 proposed that parents should vary the sex of their offspring according to their ability to invest, many studies attempted to prove that observed sex ratio variations

are

adaptive.

Mariko Hiraiwa-Hasegawa is at the Institute of Natural Science, Senshu University. 2-l-1, Higashimita. Tama-ku, Kawasaki, Kanagawa. 2 I4 lapan. 0

1993, Elsewer

Science

Publishers

Ltd (UK)

Stygologia

3, 345-372

13 Howarth, F.G. ( I98 I ) 8th lnt. Congr Speleology, 539-54 I 14 Kane, T.C. and Richardson, R.C. (1985) NSS Bull. 47, 71-77 15 Culver, D.C. and Fong, D.W. ( 1986) Stygologia 2, 208-2 I6 lb Romero, A. I 1985) NSS Bull. 47, 86-88 17 Paulson, T.L. (1985) NSSBull. 47, 109-I I7 18 Pot&on, T.L. and White, W.B. (1969) Science l65,97 I-98 I I9 Culver, DC. and Paulson, T.L. (1971) Am. Midl. Natur. 85, 74-84 20 lones, R. and Culver, D.C. (I 989) Evolution 43, 688-693 21 Marmonier, P. and Danielopol, D.L. ( I9881 Vie Milieu 38, 35-48 22 Gould, S.J. and Vrba, E.S. (I 982) Paleobiology 8, 4-I 5 23 Danielopol, D.L. et al Am. Water Res.

Assoc. (in press) 24 Dole-Olivier, M.I and Marmonier. P (I 992) Hydrobiologia 230, 49-61 25 Palmer, M.A., Bely, A.E and Berg, K.E. ( 1992) Oecologia 89, 182-l 94 26 Kane, T.C. and Brunner, GD f 1986) Psyche93, 231-251 27 Crouau-Roy, 8. (1989) Genetics 121,571-582 28 Botosaneanu, L , ed. ( 1986) Stygofauna Mundi, E.1. Brill 29 Pesce, C.L. II9921 Fragm. Entomol. Roma 24, I-12 30 Noss, R.F. (I 992) Conserv Bio/. 4, 355-364 31 Chapin, F.S., III, Schultze, E.D. and Mooney, H.A. I 1992) Trends fcol Evol 7, 107-l 08 32 Dole-Olivier, M.j. and Marmonier, P. I 1992) Stygologia 7, 65-75 33 Walker, B.H. (1992) Consew. Biol6, 18-23 34 Pospisil, P. and Danielopol. D L. (1990) Stygoiogia 5, 75-85

Skewed Birth Sex Ratios in Primates: Should High-ranking Mothers have Daughters or Sons? Mariko Hiraiwa-Hasegawa Numerous studies on sex ratio biases in nonhuman primates have been published (Table I). However, those results were sometimes contradictory and completely opposite directions of biases were reported even among populations of the same species. Adding to this confusing situation, several alternative adaptive explanations for these sex ratio variations were presented. The four main hypotheses presented so far are (I) the Trivers-Willard hypothesis, (2) the advantaged daughter hypothesis5s6, (3) the local resource competition (LRC) hypothesis at the population leve17, and (4) Silk’s local resource competition hypothesiG. On the other hand, quite a few studies could not detect any consistent sex ratio variations and some of the authors asserted that observed sex ratio variations might be mere stochastic errors. The Trivets-Willard hypothesis Trivers and Willard4 made the following assumptions: ( 1) the condition of the young at the end of parental investment (PI) will tend

to be correlated with the condition of the mother during the PI; (2) differences in the condition of young at the end of the period of PI will tend to endure into adulthood; and (3) adult males will be differentially helped in reproductive success by slight advantages in condition. Male reproductive success is expected to vary more than female reproductive success, and slight advantages in condition should have disproportionate effects on male reproductive success. If so, it follows that an adult female in good condition should produce sons who will leave more surviving grandoffspring than daughters in the same condition, while an adult female in poor condition should produce daughters who will suffer less disadvantage than sons in the same condition. Almost perfect supporting evidence for this hypothesis came from a study of red deer (Cervus e/&us) in the Isle of Rhum, UK9. In this population, high-ranking mothers tend to produce more sons, while low-ranking mothers tend to produce more daughters. The 395