CAVE AND KARST SCIENCE Vol. 36, No.

2, 2009 (published in 2010) Transactions of the British Cave Research Association

British Cave Research Association 2010 ISSN 1356-191X

Are all caves ecotones?

Max MOSELEY
90/9 Soi 49, Saiburi Road, Amphoe Muang, Songkhla 90000, Thailand. e-mail: maxmoseley@hotmail.com
Abstract: It is proposed that the ecological concept of an ecotone (a zone of steep environmental gradient between adjacent ecological communities or ecosystems) could be applied to caves in their entirety. Arguments are given in support of this proposal, and some of the conceptual, theoretical and empirical implications are highlighted and briefly discussed. Keywords: caves, zonation, ecotones, communities (Received 16 December 2009; Accepted 26 February 2010) Acce

There has been intermittent interest in the areas of transition, now known as ecotones, situated at the boundaries between relatively homogeneous ecological communities since the end of the 19th century (Clements, 1897). Although this early interest subsided after 1970 because ecologists were at that time tending to focus more on sampling and characterizing distinct homogeneous ecosystems and communities, they are now attracting much more attention because of the increasing research interest in biodiversity and on landscapes as a whole. Ecotones become conspicuous components when ecosystems are viewed at the landscape scale (Kark and van Rensburg, 2006). It has been shown that they are important in regulating ecosystem material flows and processes, and there is also evidence that they are high in biological diversity and might be speciation hotspots (Risser, 1993; Kark and van Rensburg, 2006) Recognition that ecotones can be identified in the subterranean realm is more recent and there have been relatively few investigations. It was only during the last half century that the biological significance of the range of transition zones that interconnect terrestrial and aquatic hypogean habitats with those on the surface (epigean) and with deep soils (endogean) became fully apparent, and it was not until the late 1980s that the ecotone concept was adopted for any of these. This was to groundwater/surface-water transition zones (Naiman and Dcamps, 1990). The concept has also subsequently been used in relation to some other underground transition zones, including those within cave thresholds (Simon and Benfield, 2001; Prous et al., 2004; Sharipova and Abdullin, 2007). Recently Moseley (2009a) suggested extending the concept by also applying it to caves in their entirety, hypothesising that all caves might constitute ecotones between adjacent hypogean, epigean and/or endogean communities. This proposal is developed and further justified in this essay and some of the conceptual, theoretical and empirical consequences are briefly discussed. In the following text, cave is to be understood in the sense of Moseley (2009b) as: a natural or artificial cavity in rock in which large-scale scalar phenomena are actually or potentially ecologically significant. These phenomena include the presence of surfaces (which may be at rockair, rockwater and/or waterair interfaces) available for utilization by mesofauna and/or macrofauna. Usually, though not invariably, they also include the presence and effects of fluid flow (air currents, streams, springs or tidal flow) and they also commonly have accumulations of bulk substrates such as guano, vegetable debris, talus and sediments. There is also potential for access and utilization by flying animals (bats, birds and insects) and by terrestrial and aquatic animals that are unable, because of their size, to utilize mesocaverns or smaller voids. Thus, defined in this way the term is not being used synonymously with other (smaller) subterranean voids, and in practice includes only macrocaverns and the larger mesocaverns.

What are Ecotones?

Where two substantively different ecological communities are juxtaposed, the frontier is rarely sharp or abrupt. Instead there is a zone of transition that cannot be classified as belonging exclusively to either of the adjacent communities but has characteristics of both. Such zones of transition between ecological communities are familiar to everyone. Examples are the littoral zones at the edge of the sea, lakes and other bodies of water; the boundary between forest and grassland; and the mangrove-forest/tidal-marsh transition. Although the concept had been recognized and described much earlier (Clements, 1897) it was not until the middle of the 20th century that many ecologists began to see these transitional regions as important. This was largely due to the work of Odum (1953) who coined the term ecotone to refer to them. Odum defined an ecotone as: a transition between two or more communities; it is a junction zone or tension belt which may have considerable linear extent but is narrower than the adjoining communities areas themselves [current authors underlining]. It is now known that ecotones can be recognized and defined at any spatial scale, from continental-scale transitions between major biomes (e.g. the African Sahel Region), to the zones between ecological communities such as the examples given above, and down to small-scale local transitions between different vegetation types (Weins et al., 1985; Naiman and Dcamps, 1990; Risser, 1993; Kark and van Rensburg, 2006). The characterization of ecotones based upon their geographical narrowness has been widely accepted and used: a more recent definition, which is very similar to that of Odum (1953), is: a narrow ecological zone which possesses a mixture of the floristic and faunistic characteristics in between two different and relatively homogenous ecological community types (Allen and Starr, 1982) [current authors underlining]. Placing emphasis on narrowness as a characteristic of ecotones is however, as such, potentially misleading. It arose historically because those habitats that were first identified as ecotones were essentially two-dimensional landscape features. The observed narrowness is not in itself a significant or fundamental attribute; it is a manifestation of the underlying steep (rapidly changing) environmental gradients within the ecotone. One definition that recognizes this subtle distinction is that of Kark and van Rensburg (2006 p.32): ecotones are areas of steep environmental transition along an environmental gradient, where the environment rapidly shifts from one type to another based on abiotic (i.e. climatic) and/or biotic factors. This refined definition also recognizes the important fact that their location and characteristics can be shaped by both biotic and abiotic factors (Fortin et al., 2000). Both this and the fundamental concept of a relatively steep environmental gradient are important points when the concept of ecotones is extended into a third spatial dimension in the subterranean milieu and to caves. Accordingly, this is the definition adopted in the present essay. 53

Ecotones show not only a mixing of characteristics of the adjoining communities but have additional special characteristics of their own. As habitats in their own right, they can have unique properties. It is believed for example that they have a strong tendency (referred to as the edge effect) for increased species diversity and density (Odum, 1953). This has long been recognized by wildlife managers; the early habitat management literature is replete with examples of the value of edge or margin habitats (Risser, 1993). It has also been suggested that they can support unique ecotonal genotypes and species (e.g. Odum, 1953) and it has been proposed that they might sometimes be active regions of speciation (e.g. Levin, 1993). Recent research perspectives have also drawn attention to the dynamic aspects of these ecological boundaries: an ecotone is not a static zone of contact between two communities, but a dynamic zone that changes with time and has particular properties (Lvque, 2003, p. 179). An ecotone may be a net source of energy (organisms, logs, nutrients, etc.) or a net sink. Ecotones act as ecological filters, differentially allowing the exchange of organisms and materials between adjacent ecosystems. In contrast, they may also act as barriers, isolating these ecosystems in various ways. Kolasa and Zalewski (1995) provide both a list and a useful discussion of these various functions.

Subterranean Ecotones
Historically, although a century ago Racovitza (1907, pp.384386) was already emphasising the importance of les fentes troites (narrow cracks) in limestone as habitat for cavernicoles, the biological study of the underground realm was almost entirely restricted to accessible caves and it is only in recent decades that its vast extent and ecological heterogeneity have become more fully appreciated and understood (Moseley, 2009b). Accordingly recognition of the existence

of significant subterranean ecological transition zones did not emerge fully until after 1960, and current knowledge of them remains limited and fragmentary. To date most attention has been paid to aquatic habitats, particularly those related to continental groundwater/surface-freshwater transition zones (Fig.1). This is due to a great extent to the economic importance of groundwater, especially in karst regions. Most of the relevant studies have been undertaken in mainland Europe. Orghidan (1959) and Schwoerbel (1961) were two pioneers who described the hyporeic zone at the interface of phreatic aquifers and rivers and streams where there is an exchange and mixing of water between benthal water and the phreatic water (Type 3 Fig.1). This zone ranges from a few decimetres to around a hundred metres in depth (Lvque, 2003). Perched aquifers, especially the epikarst (or subcutaneous zone) (Type 1 Fig.1), within the uppermost layers of rock are extensive features at the landscape scale. Epikarst is more or less continuous and nearly universal in karst areas at this scale (Williams, 2008; Culver and Pipan, 2009b). On the other hand, another type of perched aquifer, hypotelminorheic habitats, do not form where there is good drainage, so they are uncommon in karst landscapes but can occur in a variety of other geological settings (Culver and Pipan, 2009b). First described in the 1960s (Metrov, 1962) hypotelminorheic habitats are persistent shallow sub-surface wet spots fed by subsurface water in a slight depression and restricted in areal extent (Culver and Pipan, 2009a). They have subsequently been investigated both in Europe and in the United States (Culver and Pipan, 2009b). Other groundwater/surface-water transition zones include stream sinks and springs (risings) (Type 2 Fig.1), lake bottom streamsinks (Type 4) and areas of infiltrating lentic water (Type 5).

Figure 1: The main types of continental groundwater/surface-water ecotones. Type 1: Epikarst. Type 2: Stream sink or spring (rising). Type 3: Stream underflow. Type 4: sinkstream beneath lake. Type 5: Infiltrating lentic water. [Modified after Naiman and Dcamps, 1990, Figure 10.1.]

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Following the discovery of their taxonomically remarkable and zoogeographically important faunas, recent decades have also witnessed increasing research aimed at identifying and describing coastal marine/freshwater transitional anchialine habitats. The initial work on these was that of Riedl (1966) who described anchialine caves in Europe which he called marine Randhhle (marginal caves). They have subsequently been identified and investigated in the tropics and sub-tropics in many parts of the world (e.g. Culver and Pipan, 2009a). Interstitial marine/freshwater transitional habitats are also present and widespread in sands and gravels. Appreciation of the biological importance of terrestrial subterranean transition zones is more recent, and their investigation has lagged well behind that done on either fresh or marine subterranean waters. The Milieu Souterrain Superficiel (MSS), which consists of the network of mesocaverns within the fragmented bedrock at the base of the regolith, together with ecologically similar habitats such as talus slopes and Kaltlcher, was only recognized about thirty years ago (Juberthie et al., 1980; Juberthie, 1983). European Alpine Kaltlcher are sites cher where cavernicolous and psychro-hydrophilous organisms are found associated with stable, cold habitats in cavities in scree or solid rock (Punz et al., 2005). Organisms such as millipedes and woodlice collected along with aquatic epikarst species from drips inside caves are interpreted as evidence for a terrestrial epikarst fauna (Culver and Pipan, 2009a, p.182). The relationship between this habitat and the MSS is somewhat unclear, and they undoubtedly overlap in nature. It has been suggested that the latter is mainly confined to areas of rubble or well-developed rock fracturing and moderate to high slope, whereas the epikarst habitat consists of the extensive systems of smaller voids within the upper rock strata (Culver and Pipan, 2009a, p.183) (Fig.2). Although knowledge of the existence of these various zones of transition and increasing awareness of their wide geographical distribution, extent and ecological significance had by then been growing for almost three decades, explicit adoption of the ecotone concept as a conceptual framework for studying and understanding these hidden underground zones did not begin until little more than twenty years ago.

It was not until the late 1980s that the first application of the concept was made underground. This was to the various boundaries between groundwater and surface freshwaters. It originated within the context of the new ecosystems approach to groundwater ecology being developed by European researchers since the 1970s (Danielpol and Griebler, 2008) and this development occurred in parallel with increasing interest also being shown in ecotones by the wider ecological research community (Kark and van Rensburg, 2006). The concept was firmly established in the widely-cited book edited by Naiman and Dcamps (1990) and there has subsequently been considerable empirical work undertaken in Europe within the framework of major multi-disciplinary research programmes including the multinational PASCALIS research consortium (Gibert, 2005). The concept has, however, not yet been significantly extended beyond its application to continental subterranean groundwaters. Gers (1998) proposed a terrestrial soil to cave ecotonal gradient through the MSS. In the same year Boxhall and Jaume (1998) noted in passing that certain littoral caves and submarine caves can be considered as ecotones between the open sea and true anchialine systems. More recently the concept has been applied by a few authors to zones within the entrance regions of caves (Simon and Benfield, 2001; Prous et al., 2004; Sharipova and Abdullin, 2007).

Caves as Zonal Environments

Caves (at least those that have an entrance) are strongly zonal environments (Fig.2). The generally recognized zonation pattern is primarily defined by the attenuation of abiotic surface factors with increasing distance from the entrance. It is not surprising that the earliest investigators considered darkness of the habitat to be the single most important of these factors (Sket, 2008) and this view persisted widely, unchallenged until fairly recently. Cave biologists generally recognized only three major zones, defined by light: (a) the threshold extending from the entrance of the cave to the farthest limit of illumination sufficient to support vascular green plants; (b) the deep threshold (or twilight) zone from the inner edge of the threshold to the

Figure 2: Visualization of idealized subterranean terrestrial ecotones. The vertical soil to fissures ecotone through the MSS exists both on karst and on non-karstic rocks [SP = soil profile; MSS = regolith/Milieu Souterrain Superficiel; SCZ = subcutaneous zone (epikarst)]. Ecologically, caves constitute another type of ecotone: the surface to fissures ecotone through the cave [th = threshold; d.th = deep threshold; tsz = transitional subzone; dc = deep cave; sasz = stagnant air subzone.]. Note that entranceless caves may exist as outliers of the cave ecotone. The existence of isolated patches is neither unique nor unusual and they are common in epigean situations (see Kolasa and Zalewski, 1995, Fig.1, A). [Refer to the text for a more detailed explanation.]

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start of the dark zone; and (c) the dark zone, which is the region of the cave in perpetual darkness (Howarth, 1993). Traditionally the edge of the cave dark zone has been taken as marking the outer boundary of the hypogean (which implies that cave thresholds are epigean habitats). Except for the obvious diurnal and seasonal changes in light levels, the extent and boundaries of these zones are essentially static physical features of each individual cave. Increasing understanding of the zonal nature not just of the threshold but of those areas in perpetual darkness is a significant more recent insight. Due to their size and in most cases relative proximity to the surface, the influence of surface environmental factors in caves extends well beyond the limits of light penetration. Except where sharp physical discontinuities form barriers to air movement, these factors represent a continuous environmental gradient and accordingly the cave dark zone is, strictly speaking, clinal rather than zonal. They are also less static than light levels, changing and shifting with the seasons or with major climatic events (Howarth, 1993). However, although their boundaries are of necessity defined somewhat arbitrarily and vary over time, some cave biologists have usefully subdivided the dark zone into subzones. Working in the dry and essentially linear lava tube caves of the Hawaiian islands and a blind-ended foul air cave in Australia, Howarth (1988; 1993) observed a mainly though not exclusively, abiotic environmental gradient within the dark zone. Using these environmental parameters he subdivided the terrestrial dark zone into three subzones: (1) Transition (sub)zone: a dynamic area in total darkness (but) where the microclimate is affected by short-term meteorological effects on the surface; Deep cave (sub)zone: an area which remains relatively (environmentally) stable, characteristically with the air near moisture saturation. Air exchange with the surface keeps the air fresh. Stagnant air (sub)zone: an area where air is exchanged with the surface only slowly, relative humidity remains at 100%, while carbon dioxide and oxygen concentrations may fluctuate dramatically from decomposition of organic material.

are still biologically differentiated from mesocavernous fissures by ecologically significant scalar phenomena. Although there is as yet little direct empirical evidence in support of this, areas of rock surface are obviously present, and large measured variations in carbon dioxide and oxygen concentrations resulting from decomposition processes in sites believed to be stagnant air subzones (Howarth and Stone, 1990) do imply the presence there of organic substrates in bulk.

Caves as Ecotones
Based upon the foregoing it would appear evident that in their entirety caves ecologically are environmental and faunistic transitional regions between the surface on the one hand and the host rock fissure system on the other, characterized by a relatively steep gradient of mainly (though not exclusively) abiotic factors i.e. they are ecotones, meeting the definition of Kark and van Rensburg (2006) quoted above. Acceptance of this requires a reversal in perspective from the longstanding traditional viewpoint that the mesocavernous voids are merely an extension of the (humanly explorable) cave habitat. Instead it requires visualizing the enormous interconnected network of smaller spaces mesocaverns and microcaverns as constituting the real subterranean world, whereas the larger voids that we call caves are to be seen as transitional marginal habitats between this vast hypogean biome and the outside epigean world. Certain objections may be raised here in attempts to support a case that caves cannot be considered ecotones and accordingly must continue to be seen as habitats in their own right. The first is that the great length of some caves, sometimes tens of kilometres, means that there is no steep gradient. A second predictable objection is that caves are ecologically highly heterogeneous, supporting mosaics of different habitats rather than a simple well-defined gradient. These objections can readily be met when it is realized that both fail to take scale into account. Ecotones exist at all spatial scales. They are characterized and must be defined at the scale of the particular ecological phenomena under study (Risser, 1993). Absolute size is not in itself a significant factor. The African Sahel regional ecotone is hundreds of kilometres in width. It is the relative steepness of the gradients within the ecotone compared with adjacent regions that is diagnostic. This also means that there is no conflict between a caves as ecotones model and recognition that, for instance, a cave threshold or the hyporeic zone beneath an underground cave stream are themselves ecotones. Secondly, all ecotones are habitats and, subject to the scale and nature of the phenomena being studied, can be treated as habitats in their own right. A marine littoral zone with a mosaic of algae-covered rocks; areas of mud, sand, gravel and/or pebbles; rock pools; and various other habitats provides a good example. Applied to caves in their entirety it has to be admitted that the ecotone concept is largely dependent upon a premise that the primary habitat of the majority of cave species is a vast biome consisting of the mesocaverns and smaller voids, and that they enter caves only by accident or where and when the environment is suitable. This seems, however, now to be well-established for aquatic fauna and, whilst not yet accepted by all speleo-biologists, it is also widely conceded in the case of terrestrial biota. The convincing arguments advanced by Racovitza (1907) that it must be the case have certainly not been invalidated, and it is supported by a number of more recent authors (e.g. Howarth, 1982, 1983; Juberthie, 1983; Ueno, 1987; Oromi et al., 1991; Hamilton-Smith, 2001). The almost exclusive contribution of abiotic factors in creating the environmental gradient within the cave ecotone is worth emphasizing. Epigean ecotones are almost everywhere accompanied, or indeed defined, by changes in vegetation, which is not the case within caves except in the threshold. The environmental gradient within caves is defined by light levels, temperature, relative humidity, carbon dioxide concentration and the physical scalar phenomena already mentioned. This might be one of the reasons behind the past failure to recognize the ecotonal nature of caves. Another factor, it is suspected, is the sharp morphological contrast with traditional ecotones. Whereas the ecological gradients within ecotones on the surface occur horizontally across relatively narrow zones, those underground such as the MSS and hyporeic zones are more or less vertical gradients through relatively

(2)

(3)

In practice, the existence of a putative stagnant air region in an explored cave almost always depends on a topographical discontinuity forming a barrier to air movement (Howarth, 1993) and in consequence these are unusual features in known caves and have only been reported in a few special cases. In fact, whereas the existence of a transition region with variable conditions and of the relatively environmentallystable deep cave is hardly a matter of debate, the existence anywhere of stagnant air regions as stable permanent features has not yet been demonstrated by long-term measurements (Culver, pers. comm., 2009). However, there seems to be no theoretical reason to reject the probability and they may certainly be surmised to exist commonly in deep air-filled caves lacking an entrance of any significant size (Howarth, 1993). It is certain that there are many such entranceless karst caves (Curl, 1999). Howarth and Stone (1990) hypothesized that environmental conditions in stagnant air subzones at their study sites corresponded to those of the mesocavernous fissures within the host rock. The implication of this is that ecologically the regions of stagnant air and the mesocaverns are to all intents and purposes the same. Recently, however, Moseley (2009b) has drawn attention to the crucial ecological significance in caves of scalar (scale dependant) phenomena including relatively rapid fluid flow (air currents, streams, tidal flows), the accumulation of bulk substrates such as guano and talus, and the presence of extensive surfaces as habitat. The latter include rock surfaces (e.g. cave walls), pool surfaces and (not mentioned by Moseley 2009b) hygropetric habitats (Sket, 2004). These have substantive consequences that differentiate the larger spaces that we call caves physically and environmentally from smaller voids; play crucial ecological roles underlying much of the ecology that is actually observed in caves, but not in smaller voids; and have recently been used as the basis for the novel ecological definition of cave that is quoted above and used herein (Moseley, 2009b). It follows that, even if all other conditions are identical, stagnant air regions within caves 56

shallow layers existing in three spatial dimensions (Fig.1). Within a cave, however, there is an even greater distinction in that the gradient exists primarily along the linear axis of the cave i.e. the ecotonal gradient is much longer than it is wide (Fig.2). A consequence of the adoption of the concept of ecotones within the three-dimensional subterranean milieu from the essentially twodimensional regions on the surface is an increased expectation in certain circumstances of multiple intersecting ecotonal gradients. Gers (1998) for example proposed a vertical soil to cave ecotone through the MSS. It is clear though from the text of the paper that this author lumped caves and the mesocavernous fissure habitat together. As argued herein this should not be done. It is proposed instead that in the case of shallow near-surface caves there are two ecotonal gradients a soil to mesocavernous fissures ecotone through the regolith and subcutaneous zone, and the cave surface to fissures ecotone through the cave itself (Fig. 2) and in some situations these can intersect. It should be noted that multiple ecotones do also occur on the surface, although they have received little attention (Kark and van Rensburg, 2006). It is also very important to recognize the possibility that cave ecotones are essentially independent, local features. This means that they constitute transition zones within an individual cave or cave system between adjacent hypogean and epigean (in some cases also/or endogean) ecosystems, and harbour species common to both. Hence cave occurrences of the same species might usually reflect only the external geographical range of those species rather than any cave environment continuum. This has profound implications for the caves as islands model (Culver, 1970). It will be apparent, at first sight at least, that the idea that caves themselves are zoogeographical islands is in stark contrast with the proposal that they are ecotones. If the latter, then it follows that for the majority of species found in them caves probably represent not isolated virtual islands but the periphery of their ecological range; whether that lies primarily within epigean, endogean or hypogean habitats. Certainly, it is now accepted that the evidence for the islands model is rather weak and that it is rather at the larger scale of contiguous karst areas that there is a physical and biological analogy with oceanic islands (Culver and Pipan, 2009a, pp.162 and 165) and, 2009a given this, there seems to be no conflict between this interpretation and the proposed caves as ecotones model. On the other hand the local, individual nature of cave ecotones will if true point back towards there being some degree of ecological isolation of individual caves or cave systems and this in turn might have a bearing on the oft-reported high level of endemism and frequency of cryptic species in these habitats (Culver, 2008). Acceptance of the caves as ecotones concept does not depend on taking a position such as that advanced by Karaman (1954) that there are no true cave species. The existence of specialized cave-associated species such as the sympatric cave-restricted fishes Schistura oedipus and Cryptotora thamicola of northwestern Thailand, and specialized threshold-dwelling cave spiders such as Meta spp. (all discussed in Moseley, 2009b) might, in fact, lend support to the currently unresolved general question within ecology of the existence of true ecotonal species.

Adoption of the concept of caves as ecotones thus not only places them as integral ecological components of the larger karst ecosystem, but offers the additional major advantage of shifting the focus from one in which they are central and representative, to a more valid one in which caves are not only distinguished from the rest of the subterranean, but are demoted from their central position to that of peripheral transitional habitats within a much larger ecological context. The empirical difficulties to be faced in investigation of cave ecotones must not, however, be understated. The basic description of the faunas found living in caves remains highly imperfect; knowledge of the species diversity even in the few well-sampled examples anywhere in the world is incomplete (Culver, 2008). Much less is known about the diversity and ecological and other relationships between these animals and those of adjacent subterranean and surface habitats. Because of the great difficulty of sampling the extensive networks of smaller voids, there is very little direct information available about their inhabitants. Perhaps somewhat surprisingly, and certainly ironically, it is also the case that, imperfect as it undoubtedly is, knowledge of cave-associated fauna is commonly far better than that of nearby epigean (surface) communities. This was pointed out by Hoffman (1978) in the case of millipedes, and similarly with reference to North American aleocharine beetles by Klimaszewski and Peck (1986). It is worth noting here that speleo-biologists working in those geographical areas such as the British Isles where the epigean fauna is relatively well-known might thus be advantaged in this respect. However, despite the difficulties, the potential benefits might be great. Conceptualization of caves as ecotones offers a radical new perspective with potential relevance to many of the unresolved questions about the ecology, biogeography and evolution of subterranean fauna. It ought, for instance, to prove of great value in the development of integrated ecosystems approaches to understanding the ecology of subterranean terrestrial communities. Insights gained from studies of other ecotones might lead to novel insights into the ecology and evolution of organisms found in caves and these might in turn elucidate and inform understanding of ecotones in general. Because of the dominant contribution of fairly simple abiotic gradients, it is possible that caves (sensu Moseley, 2009b) might prove to be better empirical models of ecotones than the ecologically more complex examples found on the surface. What role do these transitional habitats play in the initial colonization of the subterranean milieu; and in persistence, adaptation and speciation of hypogean organisms? The model might also lead to explanations of the high levels of genotypic and species diversity apparently to be found in cave communities compared with those in adjacent communities. Finally, a caves as ecotones model has profound implications for the conservation and management of cave-associated faunas. By placing caves firmly within and dependent upon contiguous ecosystems it brings into sharp focus the fact that the protection and management of those ecosystems is an essential consideration in the conservation of cave-associated faunas. The common existence in caves of unique genotypes or cryptic species is also a related and important conservation issue.

Acknowledgements
My sincere thanks go to David Culver, Lee Knight, Boris Sket and Paul Wood for reading early versions of this essay, raising objections that certainly needed to be addressed, and suggesting improvements. I am further grateful to David Culver for sending me a copy of the full text and English translation of Racovitzas delightful 1907 Essai. Ajarn James Staley (Thaksin University, Songkhla, Thailand) kindly helped with preparation of Fig.2.

Concluding
Future progress in understanding the ecology of caves is very likely to depend upon the adoption of a holistic ecosystems approach, as has been done so successfully in groundwater ecology by European researchers. When viewed as components within landscape-scale ecosystems, there seems little doubt that at this scale caves can and should be defined and investigated as ecotones. Ignorance of the composition, extent and significance of the faunas of subterranean habitats other than caves, and the extreme problems involved in their sampling and investigation (both undoubtedly greatly exacerbated by the cognitive difficulty of escaping from a human cave-centred perspective) means that caves have long been used by biologists as a proxy for these other habitats. The presupposition, almost invariably unstated, that they could be used in this way was expedient and understandable but now, with increasing knowledge of the subterranean milieu as a whole, and a slowly emerging understanding of the true place of caves within it, it can now no longer be justified.

References
Allen, T F H and Starr, T B. 1982. Hierarchy: Perspectives for Ecological Complexity. [Chicago: University of Chicago Press.] 310pp. Boxhall, G A and Jaume, D. 1998. On the origin of misophriod copepods from anchialine caves. Crustaceana, Vol.72(8), 957963. Clements, F E. 1897. Peculiar zonal formations of the Great Plains. American Naturalist, Vol.31, 968970. Culver, D C. 1970. Analysis of simple cave communities. I. Caves as Islands. Evolution, Vol.24, 463474. Culver, D C. 2008. The struggle to measure subterranean biodiversity. 5459 in Martin, J B and White, W B (editors), Frontiers of Karst Research, Special Publication 13. [Charlottesville, Virginia: Karst Waters Institute.]

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Culver, D C and Pipan, T. 2009a. The Biology of Caves and Other Subterranean Habitats. [Oxford: Oxford University Press.] 256pp. Culver, D C and Pipan, T. 2009b. Superficial subterranean habitats gateway to the subterranean realm? Cave and Karst Science, Vol. 35(1+2), 512. Curl, R L. 1999. Entranceless and fractal caves revisited. 183185 in Palmer, revisited A N, Palmer, M V and Sasowsky, I D (editors), Karst Modelling, Special Publication 5. [Charlottesville, Virginia Karst Waters Institute.] Danielpol, D L and Griebler, C. 2008. Changing paradigms in groundwater ecology from the Living Fossils tradition to the New Groundwater Ecology. International Review of Hydrobiology, Vol.93(45), 565577. Fortin, M-J, Olson, R J, Ferson, S, Iverson, L, Hunsaker, C, Edwards, G, Levine, D, Butera, K and Klemas, V. 2000. Issues related to the detection of boundaries. Landscape Ecology, Vol.15, 453466. Gers, C. 1998. Diversity of energy fluxes and interactions between arthropod communities: from soil to cave. Acta Oecologica, Vol.19(3), 205213. Gibert, J (Editor). 2005. World Subterranean Biodiversity. Proceedings of an international symposium held on 8 10 December 2004 in Villeurbanne, France. Equipe Hydrobiologie et Ecologie Souterraines, Universite Claude Bernard Lyon 1, France, 182pp. Hamilton-Smith, E. 2001. Current initiatives in the protection of karst biodiversity. Natura Croatica, Vol.10(3), 229242. Hoffman, R L. 1978. Diplopoda from Papuan caves (zoological results of the British Speleological Expedition to Papua New Guinea, 1975, 4). International Journal of Speleology, Vol. 9(34), 281307. Howarth, F G. 1982. Bioclimatic and geologic factors governing the evolution and distribution of Hawaiian cave insects. Entomologia Generalis, Vol.8(1), 1726. Howarth, F G. 1983. Ecology of cave arthropods. Annual Review of Entomology, Vol.28, 365389. Howarth, F G. 1988. Environmental Ecology of North Queensland Caves. or why there are so many Troglobites in Australia. 7684 in Pearson, L (Editor), 17th Biennial Conference, Australian Speleological Federation Tropicon Conference, Lake Tinaroo, Far North Queensland, 27th31st December 1988, Cairns. Howarth, F G. 1993. High-stress subterranean habitats and evolutionary change in cave-inhabiting arthropods. American Naturalist, Vol.142 (Supplement), S6577. Howarth, F G and Stone, F D. 1990. Elevated carbon dioxide levels in Bayliss Cave, Australia: implications for the evolution of obligate cave species. Pacific Science, Vol.44, 207218. Juberthie, C. 1983. [Introduction] Le milieu souterrain: tendue et composition. M Mmoires de Biospologiques, 10, 1765. Juberthie, C, Delay, B and Bouillion, M. 1980. Extension du milieu souterrain en zone non-calcaire: description dun nouveau milieu et de son peuplement par les Coloptres troglobies. Mmoires de Biospologiques, Vol.7, 1952. M Karaman, S L. 1954. ber unsere unterirdische Fauna. Acta Musei Macedonici Scientiarum Naturalium, Skopji. Vol.1(9), 195215. Kark, S and van Rensburg, B J. 2006. Ecotones. Marginal or Central Areas of Transition? Israel Journal of Ecology and Evolution, Vol.52, 2953. Klimaszewski, J and Peck, S B. 1986. A review of the cavernicolous Staphylinidae (Coleoptera) of Eastern North America: Part 1. Aleocharinae. Quaestiones Entomologicae, Vol.22(2), 51113. Kolasa, J and Zalewski, M. 1995. Notes on ecotone attributes and function. Hydrobiologia, Vol.303, 17. Lvque, C. 2003. Ecology from Ecosystem to Biosphere. [Enfield, New Hampshire: Science Publishers Inc.] 472 pp.

Levin, D A. 1993. Local speciation in plants: the rule not the exception. Systematic Botany, Vol.18, 197208. Metrov, M. 1962. Un nouveau milieu aquatique souterrain: le biotope hypotelminorheique. Compte Rendus Academie des Sciences, Paris, Vol.254, 26772679. Moseley, M. 2009a. Estimating diversity and ecological status of cave invertebrates. Some lessons and recommendations from Dark Cave (Batu Caves, Malaysia). Cave and Karst Science, Vol.35(1+2), 4752. Moseley, M. 2009b. Size matters: scalar phenomena and a proposal for an ecological definition of cave. Cave and Karst Science, Vol.35(3), 8994. Naiman, R J and Dcamps, H (editors). 1990. The Ecology and Management of Aquatic-Terrestrial Ecotones. Man and the Biosphere Series: Vol.4. [London: Parthenon Publishing Group.] 316 pp. Odum, E P. 1953. Fundamentals of Ecology. [Philadelphia: W B Saunders Company.] 383pp. Orghidan, T. 1959. Ein neuer Lebensraum des unterirdischen Wassers, das hyporheische Biotop. Archiv fr Hydrobiologie, Vol.55, 392414. f Oromi, P, Martin, J L, Medina, A L and Izquierdo, I. 1991. The evolution of the hypogean fauna in the Canary Islands. 380395 in Dudley, E C (editor), The unity of evolutionary biology, Vol.1. Dioscoroides, Portland, Oregon. Prous, X, Ferreira, R L and Martins, R P. 2004. Ecotone delimitation. Epigeanhypogean transition in cave ecosystems. Austral Ecology, Vol.24(4), 374 382. Punz, W, Sieghardt, H, Maier, R, Engenhart, M and Christian, E. 2005. Kaltlcher im Ostalpenraum. Verhandlungen der Zoologisch-Botanischen Gesellschaft in sterreich, Vol.142, 2745. Racovitza, E G. 1907. Essai sur les problemes biospeologiques. Archive de Zoologie Experimentale et Generale (Biospeologie I), 4e serie, 6, 371 488. Riedl, R., 1966. Biologie der Meereschhlen. [Hamburg: Verlag Paul Parey.] 636pp. Risser, P G. 1993. Ecotones at local to regional scales from around the world. Ecological Applications. Vol.3(3), 367368. Schwoerbel, J. 1961. Subterrane Wassermilben (Acari. Hydrachnellidae, Porohalacaridae und Stygothrombiidae), ihre kologie und Bedeutung fr kologie f die Abgrenzung eines aquatischen Lebensraumeszwischen Oberflche und Grundwasser. Archiv fr Hydrobiologie, Suppl. 25, 242306. f Sharipova, M Y and Abdullin, S R. 2007. Algological investigation of cave ecotones. Siberian Journal of Ecology, Vol.14(6), 10171023. Simon, K S and Benfield, E F. 2001. Leaf and wood breakdown in cave streams. Journal of the North American Benthological Society, Vol.20(4), 550563. Sket, B. 2008. Can we agree on an ecological classification of subterranean animals? Journal of Natural History, Vol.42(21+22), 15491563. Sket, B. 2004. The cave hygropetric a little known habitat and its inhabitants. Archiv fr Hydrobiologie, Vol.160(3), 413425. f Ueno, S-I. 1987. The derivation of terrestrial cave animals. Zoological Science, Vol.4, 593606. Weins, J A, Crawford, C S and Gosz, J R. 1985. Boundary dynamics a conceptual framework for studying landscape ecosystems. Oikos, Vol.45, 421427. Williams, P W. 2008. The role of the epikarst in karst and cave hydrogeology: a review. International Journal of Speleology, Vol.37(1), 110.

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