Corresponding author: Eleonora Trajano ( firstname.lastname@example.org )
Academic editor: Oana Moldovan
© 2017 Eleonora Trajano, Marcelo R. de Carvalho.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation: Trajano E, Carvalho MR (2017) Towards a biologically meaningful classification of subterranean organisms: a critical analysis of the Schiner-Racovitza system from a historical perspective, difficulties of its application and implications for conservation. Subterranean Biology 22: 1-26. https://doi.org/10.3897/subtbiol.22.9759
Subterranean organisms always attracted the attention of humans using caves with various purposes, due to the strange appearance of several among them and life in an environment considered extreme. According to a classification based on the evolutionary and ecological relationships of these organisms with subterranean habitats, first proposed by Schiner in 1854 and emended by Racovitza in 1907, three categories have been recognized: troglobites, troglophles and trogloxenes. The Schiner-Racovitza system has been discussed, criticized, emended, the categories have been redefined, subdivided, original meanings have changed, but it is used until now. Herein we analyze in a conceptual framework the main ecological classifications of subterranean organisms, from Schiner to Trajano, in 2012, so far the last author to introduce a relevant conceptual change on the categories definitions, incorporating the source-sink population model. Conceptual inconsistencies are pointed, especially with regards to the generally ill-defined trogloxene category, and the correspondence between categories according to the original sense and in alternative classifications is discussed. Practical criteria for distinction between these categories and difficulties for their application are presented. The importance of rightly classifying subterranean populations according to the Schiner-Racovitza system for conservation of these fragile and mostly threatened habitats is discussed.
Subterranean biology, troglobites, troglophiles, trogloxenes, cave conservation
The realization that the subterranean realm contains living fauna is probably as ancient as the beginning of the regular use of caves by humans for ritual activities (ceremonies, burials etc.) during prehistoric times (
The presence of animals with very distinctive features, unfamiliar to the general public and conferring an appearance that is usually described as peculiar, bizarre and even fearsome, sometimes depicted as mixing real animals with mythic creatures such as dragons, is the most striking characteristic of the subterranean biota. And more, these creatures coexist in caves with “normal” animals, like those found on surface habitats. So it is not surprising that the first attempts to classify cave animals were based on their differences to surface inhabitants. A traditional classification, still used, is that by Schiner, published in 1854 and emended by Racovitza in 1907 (
The classification of organisms living in subterranean habitats according to their ecological and evolutionary relationships is a central issue in subterranean biology because it provides the starting point for many other questions. However, underlying concepts are not well understood and definitions of these categories have been changing through time, such that the same term is used for different situations and vice-versa. Because authors very rarely make reference to the system they used, or the practical criteria for its implementation, the general application of a classification to cave animals is frequently unreliable.
Here we present a review of the most used ecological/evolutionary classification of subterranean organisms, the Schiner-Racovitza classification, analyzing it from historical and conceptual points of view, and detail a recent proposal incorporating the source-sink population model. We also discuss practical criteria for its application and its importance for conservation of the fragile subterranean ecosystems.
According to Racovitza’s classic publication , several attempts had been made to establish divisions of the cave fauna based on diverse criteria, such as type of preferred habitat of cavernicoles. The latter criterion was used in 1854 by Schiner to classify these organisms into: 1) hôtes occasionels (occasional visitors): “animaux qu´on rencontre dans les grottes mais aussi à la surface, partout ‘wo sich die ihrer Lebensart entsprechenden Bengungen vorfinden’; 2) troglophiles (troglophiles): “animaux habitant les régions où la lumière du jour pénètre encore, qu´on peut, excepcionallement, rencontrer à la surface ou qui ont seulement des formes répresentatives lucicoles”; 3) troglobies (troglobites): “animaux exclusivement cavernicoles, qu´on ne rencontre jamais dans les regions épigées, sauf dans le cas d´événements excepcionnels comme les crues” (
A comparison of definitions of the Schiner-Racovitza categories (except for the troglobites, var. troglobionts) by different authors.
|Trogloxenes (Schiner´s hôtes occasionels = occasional visitors)||Animals found in caves, but also at the surface, everywhere ‘when one finds those constraints typical of their life style||Animals lost or occasional visitors of caves attracted by humidity or food, but that do not live continuously or reproduce in caves||Organisms that live in the suface but, due to very precise reasons, they colonize temporarily the subterranean environment (“hôtes temporaires”)||Species habitually found in caves or similar cool, dark habitats outside caves, but they must return periodically to the surface or at least to the entrance zone of a cave for food.||Subtroglophiles
Need to utilize the surface environment for at least one vital fuction (e.g,. reproduction or feeding)
|Source populations in epigean habitats, with individuals using subterranean resources|
|Troglophiles||Animals inhabiting regions where day-light still penetrates, which can exceptionally be found at the surface or that only have photophilous forms||Permanently inhabiting the subterranean domain, but preferably in superficial regions; they frequently reproduce there, but may also be found outside||Organisms that live in the subterranean environment as well as in the surface (“hôtes électifs”)||Species able to complete their life cycles within a cave but may also occur in ecologically suitable habitats outside caves||Eutroglophiles
Essentially epigean species able to establish more or less permanent subterranean populations
|Source populations both in hypogean and epigean habitats, with individuals regularly commuting between these habitats, promoting the introgression of genes selected under epigean regimes into subterranean populations (and vice-versa)|
|Accidentals||Species that wander, fall or are washed into caves and generally exist there temporarily.||Trogloxenes||Organisms introduced into caves by mishap or entering in search of a mild climate; may survive temporarily, but the inability to orient themselves and to find food leads to their eventual demise. Not evolutionary units responding to subterranean selective regimens.|
The latter category, the troglobites, is basically that of Schiner and has remained mostly unaltered to the present. On the other hand, and assuming that
In addition to creating a new term,
Since the beginning there has been a consensus about the definition of troglobites as animals confined to subterranean habitats. However, many authors, including Racovitza, mistakenly made a necessary linkage with the presence of morphological cave-related traits, termed troglomorphisms by
The absence of organisms in epigean habitats is a definition by itself, independent of the cause of the absence. At least theoretically, because there are very few experimental studies on the subject, troglomorphisms would hinder epigean life, but it is not the only possible cause for it. The maintenance of ecological, hydrological and/or geological barriers may also account for the troglobitic status (i.e. restriction to caves) without the onset of troglomorphisms (i.e. of cave-related autapomorphies).
Racovitza´s imprecise definition of troglophiles persisted in Europe until the 1960´s –
Modern, biologically meaningful definitions taking into account the Schiner-Racovitza categories were published in the late 1960´s and early 1970´s. The most important advancement was the trogloxene concept, which excluded accidentals, i.e. animals without an ecological relationship with caves (Table
The Shiner-Racovitza classification, understandably in view of its importance as a central theme in subterranean biology, has been subject to much debate and criticism in the last century. Several proposals have been elaborated, either as modified versions of the original classification, or more detailed versions with subdivisions, redefinitions, or with alternative meanings, and with new categories based on distinct criteria (
Another good example of unnecessary complication leading to classifications devoid of biological sense is the essentially theoretical system proposed by the Italian speleobiologist M. Pavan in the late 1940´s, a hierarchical dichotomous system based on the ability to live and reproduce in the subterranean environment (
Contrary to assertions by
The subdivision of troglophiles into eutroglophiles and subtroglophiles, as recently defended by
It is noteworthy that the Schiner-Racovitza system applies to organisms living in the subterranean environment in general, i.e. in networks of heterogeneous inter-communicating spaces of the subsoil, characterized by permanent absence of light, moderate annual amplitude of temperature and, for the terrestrial component, relative humidity close to 100% (
A first conceptual problem with these definitions refers to the organizational level of the categories. In many definitions the reference used is “animals” or “cavernicoles”. These terms are too vague, and may refer to individuals, populations or species. In others, the reference is the species, at least for troglobites and troglophiles, as in
Another apparent inconsistency comes from the occasional observation of troglobites in surface habitats. Schiner had acknowledged this possibility as an exceptional event, exemplified by the presence of European blind salamanders Proteus anguinus outside caves as a consequence of flash floods (
Another issue concerns groups of individuals in habitats where they would not form self-sustained populations, i.e., in habitats where reproduction would not be sufficient to balance local mortality (sink habitats). Such populations might only persist if maintained by immigration from more-productive sources, i.e., from populations with excess production that would continue to grow if isolated (source population) (
Trichomycterus itacarambiensis (Siluriformes: Trichomycteridae), troglobitic catfish from eastern Brazil, showing intrapopulation variation in pigmentation and eye development (Photos: Dante Fenolio). A pigmented individual, with reduced eyes and pigmentation B albino (DOPA (–) individual, with very reduced eyes, not visible externally.
These categories apply to subterranean organisms (cavernicoles sensu lato) defined as evolutionary units responding to subterranean selective regimens. Subterranean habitats would provide resources, e.g. food, shelter, substrate, climate, which affect survival/reproductive rates. Such units have an historical connectivity, therefore may be classified as systematically meaningful biological systems. Therefore, “accidentals”, i.e., organisms introduced into caves by mishap (by being washed into caves or falling through upper openings, for instance) or when entering in search of a mild climate are excluded; although such organisms can survive temporarily, their inability to properly orient themselves and to find food leads to their eventual demise. From an ecological point of view, accidentals are potential resources for subterranean organisms (food, substrate, etc.). Resources per se have no historical connectivity, and when an organism is just a resource, it makes no sense to classify it into a taxonomic system, based on phylogeny. Moreover, accidentals are grouped by a negative trait (i.e., they are not subterranean organisms, as herein defined). In conclusion, it is clear that the “accidental” concept has a different nature, and therefore should not be included in the Schiner-Racovitza system (
It is noteworthy that troglobites, troglophiles and trogloxenes are all subterranean, i.e., they are all adapted to subterranean life, each in their own way. It is a common mistake to refer to troglobites in the speleological literature as the cave-adapted organisms, as a distinction from other subterranean animals, i.e., from troglophiles and trogloxenes (e.g.
The origin of such errors is probably the equivocated notion that the presence of autapomorphies (such as troglomorphisms, in the case of troglobites) is a necessary condition for adaptation to certain ways of life. However, by definition, troglophiles are self-sustained (source) subterranean populations, recognizable as such and distinguishable from troglobites exactly by the lack of autapomorphies due to the introgression of genes maintained by stabilizing selection in epigean populations. In fact, vicariance models, which would explain the origin of troglobites in most cases (
Moreover, according to the neutral hypothesis for character regression, most troglomorphisms are not adaptive but neutral; the modern alternative hypothesis, that of pleiotropic effects due to selection of some beneficial traits, proposed for eye and pigmentation regression in Mexican cavefish, genus Astyanax, lacks validation from genetic studies (
The paleoclimatic model implies isolation of troglophilic populations in subterranean habitats due to exclusion of the epigean population living in the area, as a consequence of climatic changes that render surface habitats unsuitable for a species (
On the other hand, depending on the degree of differentiation achieved, the troglobitic species might or might not be able to return to the surface when environmental conditions that were previously favorable to the ancestral populations are reinstated. Therefore, conceptually there are two modalities of troglobitic status: 1) troglobites that are unable to survive in any superficial habitat, and 2) troglobites that are not found in the epigean area connected with their subterranean habitat, because the environment is unfavorable, but which could re-colonize the surface if the original conditions were to be restored. It is reasonable to hypothesize that the most specialized, highly troglomorphic troglobites are included in the first case. On the other hand, although no such case has been demonstrated so far, it is not unreasonable to suppose that among troglobites showing individual variability of troglomorphisms (Fig.
Since, especially for troglobites with intrapopulational variability, it is not possible to anticipate the level of differentiation achieved, we propose an amendment to the definition of troglobites: troglobites correspond to exclusively subterranean source populations; sink populations may be found in surface habitats, but they are unable to turn into source populations under present-day conditions.
Criticisms on the Schiner-Racovitza classification, resulting in proposals to modify or abandon it, are generally based on difficulties for its application. Most frequently, such difficulties are due to: 1) poor understanding of the conceptual framework, 2) use of inadequate methods, especially insufficient sampling effort, and/or 3) missing data on the distribution and biology of taxa of interest. By definition, troglobites are distinguished from troglophiles and trogloxenes by their geographic isolation. Hence, the primary criterion for separation of troglobites from other subterranean organisms is habitat restriction. However, it is not possible to prove an absence, only to raise its probability by repeatedly searching for the absent item, until such absence may be statistically accepted or dismissed. In our case, acceptance of a statistically significant probability of absence in epigean habitats contiguous to the subterranean one inhabited by the putative troglobite depends on extensive surveying of the surface until sampling sufficiency is demonstrated. Except for large animals, such as fishes and large arachnids, this condition is rarely achieved.
Therefore, in practice, troglobite status is recognized after morphological differentiation has occurred. It is expected that relatively small populations, isolated in environments that highly contrast with the ancestral one, present high rates of divergence (e.g.
Interrelationships between evolutionary (historical) and ecological (present-day) factors, defining the conditions of trogloxenes versus troglophiles versus troglobites for subterranean organisms.
Assigning a subterranean organism to any of these categories, a procedure that has not only scientific but also conservational consequences, is not a trivial matter. With few exceptions, it is not possible to do so with an acceptable degree of confidence after a single or a few instances of field observation, and especially without a thorough taxonomic study. Ideally, the inclusion of a troglomorphic species in the most robust phylogenetic proposal available, allowing for a more complete understanding of character evolution, would be sufficient for a well-based hypothesis of troglobitic status. One may think that if there were no other troglomorphic representative in the genus or higher-level taxa then the question would be solved. However, due to the dynamic nature of systematics, where the finding of new taxa or more detailed analyses may change ideas about phylogenetic relationships, and therefore classification, the question is never closed and troglobitic status must remain a hypothesis.
Many authors, partially following
The correlation between permanent absence of light and regression of visual structures and melanic pigmentation has been established several decades ago, indicating the same evolutionary mechanisms (e.g.
The small Brazilian prodidomid spider, Brasilomma enigmatica (
In conclusion, the morphological approach alone, not associated with extensive epigean surveys, is particularly inadequate when the objective is a conclusive classification of typical soil organisms into the Schiner-Racovitza system.
It is also noteworthy that finding troglomorphic specimens considered in epigean habits is not enough to dismiss the troglobitic status at once. As epigean individuals may be stranded in caves, and thus becoming ecological accidentals, the opposite is also true. So, this may be a case of sink population, expected according to
The separation between the troglophilic and trogloxene status is ecological, not evolutionary, since it may depend on food availability (Fig.
It is noteworthy that troglophiles are not less modified cavernicoles in a continuum of cave adaptation towards troglobites. In fact, the mosaic distribution of troglomorphic character states in several subterranean taxa demonstrates that such a continuum does not exist. Among fishes, this is well illustrated for the North-American amblyopsids (
Once a subterranean specimen is assigned to a known species or OTU, the following step is to find evidence that it belongs to a source population. In the case of non-troglomorphic subterranean animals that cannot be identified, either due to a lack of taxonomic expertise or because it is a new species (very common in tropical countries), it is especially difficult without an extensive surface survey and comparative taxonomic study to distinguish between the status of troglophile and troglobite without troglomorphisms. Because few cases of non-troglomorphic troglobites have been reported for areas where epigean habitats are relatively well known, in a first moment such animals should be considered troglophiles without further consideration, except when epigean habitats are clearly unsuitable for their survival.
Evidence of self-sustained, source populations in subterranean habitats include the presence of all age/size classes throughout the cave, throughout the year. Trogloxenes, on the contrary, are usually found not far from contacts with the surface, at distances compatible with their locomotor capacity allowing for regular commuting between epigean and hypogean habitats without losing much energy (the trade-off between the advantages of using subterranean resources, mainly for shelter, and the energy spent for movements). Moreover, several trogloxenes use caves seasonally, being absent during part of the year. Therefore, a definitive distinction between troglophiles and trogloxenes depends on populational studies conducted on an annual basis.
Among trogloxenes, recognition of obligatory trogloxenes depends on good data on biology, population ecology and distribution of the species, indicating that the epigean distribution is always correlated to the presence of rocky shelters in the area. Hadenoecus camel crickets (Rhaphidophoridae) from karst areas in Kentucky, USA, have long been recognized as obligatory trogloxenes, based on visual censuses from several seasons revealing the existence of circadian rhythms (with activity in the night phase) and analyses of food items showing that most have epigean procedence. These crickets may be found deep in caves, but usually during the reproductive phase. Also, two species of Euhadenoecus from the Appalachians are obligatory trogloxenes that must reproduce in caves but spend time in the forest, always being found in karst areas; camel crickets of two other species are forest-dwellers that may frequent cave entrances (
In Brazil, the only obligatory trogloxene so far recognized with basis on scientific data is the harvestman Acutisoma spelaeus (Fig.
Acutisoma spelaeum (Arachnida: Opilioes), an obligatory trogloxene from caves in southeastern Brazil: female taking care of eggs (Photo: Renata Nunes).
Among bats, species from temperate regions, such as Myotis sodalis and M. lucifugus, which have a relatively wide distribution in North America, are dependent on a small number of caves for hibernation (
It is important to emphasize that observation of individuals entering or leaving caves is not, per se, evidence of trogloxene status, because, as mentioned, both trogloxenes and troglophiles move across contacts between epigean and subterranean habitats, the former because they have to and the latter because they may do so. Also, isolated individuals are frequently classified as trogloxenes due to the erroneous notion that they are always rare in caves whereas troglophiles are common. Population densities are not criteria for distinction between Schiner-Racovitza classes, because this parameter is dependent on current ecological factors and presents the same range of variation for populations within each of these classes (variations in population sizes and densities are even observed within the same species, as in the troglobitic armored catfish, Ancistrus cryptophthalmus;
Another pitfall in the application of Schiner-Racovitza classification is borne from the fact that, in many cases, population densities of troglophiles are considerably higher than those of conspecific epigean populations. On the surface, where other species with similar ecological requirements are present, intraspecific competition would maintain low population densities. In caves, the absence of competitors and predators allows for greater population densities. As a consequence of low densities, and also the usually higher structural complexity in epigean habitats, sampling surface populations would demand higher collecting efforts than in caves. When epigean surveying is insufficient, troglophiles may be mistaken for non-troglomorphic troglobites or something else. For instance, not having collected epigean specimens,
Ctenus fasciatus (Arachnida: Araneae), a common troglophile in caves from southeastern Brazil (Photo: Renata Nunes).
Two biological elements of the subterranean environment that are considered quite spectacular call the attention of the general public: the bizarre looks of the most specialized troglobites and the presence of relicts, still called “living fossils”. Relicts are generally defined as troglobites without known close living relatives in the regional epigean area, either because these relatives became extinct (phylogenetic relicts) or because they were excluded from that area for some reason (for instance, due to climate change) but survived somewhere else (distributional or geographic relicts) (e.g.
Another example of the volatility of the concept of relict is the highly troglomorphic heptapterid catfish from Toca do Gonçalo, Campo Formoso karst area, Bahia State, northeastern Brazil (Figure
Even the greatest optimist knows that it is impossible to save all and each ecosystem and that many natural habitats will be lost for the sake of human interests. The goal of conservation is to minimize such losses by setting priorities based on scientific criteria that take into account the relative importance of areas in terms of biodiversity representativeness, not only in terms of diversity (taxonomic, phylogenetic, ecological) but also in relation to the processes that produce it. Therefore, one of the main focuses of conservation is singularity, i.e., sets of exclusive characteristics accountable for biodiversity loss if the ecosystem is irreversibly impacted.
Due to their many particularities, and although normally presenting taxonomic diversities considerably lower than that observed on the surface, subterranean ecosystems are generally characterized by high phylogenetic, morphological and functional diversities (
There are enough reasons justifying the protection of all subterranean organisms, but troglobites and obligatory trogloxenes are matters of greater concern, not only because of their higher degree of singularity (especially the former), but also in view of their much higher vulnerability to environmental disturbances due to their dependence on the integrity of a fragmented, frequently spatially restricted and intrinsically fragile environment (e.g.
The main challenges facing conservation of subterranean populations are: 1) to distinguish accidentals, which have no importance for conservation at all, from subterranean organisms with low population densities that require large areas for maintenance of minimum viable effective populations; it is noteworthy that sparse populations and/or small ranges, a frequent trait of troglobites, are conditions in two out of three ecological axes (habitat requirements, local abundance and geographic range) which, combined, result in the seven Rabinowitz´s forms of rarity conferring priority for conservation (
Classifying subterranean organisms according to a biologically meaningful, unambiguous, consistent Schiner-Racovitza system is highly relevant for the preservation of fragile subterranean ecosystems because it will direct conservation policies. Such policies are based on speleobiological studies which, to be reliable for this purpose, should incorporate methods allowing for a more clear distinction between the Schiner-Racovitza classes.
For many subterranean populations, caves are only part of their natural habitat. These animals may migrate between large caves and the network of small spaces around them on seasonal and/or non-seasonal bases (
Since its first proposition, in the mid 1850´s, the Schiner-Racovitza system of classification of subterranean organisms, primarily with three categories based on their ecological-evolutionary relationships with the hypogean environment, has been subject to much debate, criticism and redefinitions. Therefore, it is always necessary to make reference to the system followed.
Aiming at a biologically meaningful classification, which would account for the apparent observed inconsistencies,
Troglophiles are not less modified cavernicoles in a continuum of cave adaptation, with troglobites at the extreme end; troglophiles and troglobites are equally adapted to the subterranean life.
Troglobites and obligatory trogloxenes are especially fragile because they depend on the integrity of the subterranean habitat for their survival. Therefore, determination of their status is relevant for conservation purposes.
Major difficulties and pitfalls in the application of the Schiner-Racovitza classification are: separation of subterranean organisms (defined as evolutionary units responding to subterranean selective regimens) from accidentals; use of troglomorphisms to infer the troglobitic status; distinction between troglophiles and trogloxenes; detection of obligatory trogloxenes. In order to overcome such difficulties and avoid the pitfalls, one should take into consideration the following points:
A regular use of subsurface habitats is the first criterion to distinguish subterranean organisms from accidentals, thus isolated observations are insufficient. Repeated observations, supported by data on distribution, ecology and biology of the taxa of interest, are needed for a conclusive classification into the Schiner-Racovitza system.
The use of troglomorphisms, such as the reduction of visual organs and dark pigmentation, to infer the troglobitic condition requires the comparative method in order to confirm their autapomorphic state.
Distinction between troglophiles and trogloxenes is not trivial because in both cases individuals move between the subterranean environment and the surface. Evidence of subterranean source populations characterizing the first ones includes the presence of all age/size classes throughout the cave, throughout the annual cycle.
Except for mammals and birds, for which the high energetic demands of endothermy naturally implies the trogloxenic status, to establish this condition is usually difficult because it requires demonstrating that each individual leaves the subterranean habitat in a cyclical way. Thus, for a conclusive classification, long term ecological studies using a chronobiological approach are necessary.
Recognition of obligatory trogloxenes depends on good data on biology, population ecology and distribution of the species indicating that the epigean distribution is always correlated to the presence of rocky shelters in the area.
The condition of relict (taxon without living epigean relatives) may be an artifact of the state-of-art of the group systematics and biogeography, hence it must be treated with caution.
The dynamics of troglophilic populations may be different from that of epigean populations, with higher densities observed in caves. Collecting efforts in epigean habitats even higher than in the subterranean ones may be required to distinguish between non troglomorphic troglobites and troglophiles with very low population densities in the surface.
A robust, consistent conceptual framework is very important for a proper application of the Schiner-Racovitza ecological classification of subterranean organisms. Misplacing these organisms within these categories impairs the efficiency of conservation policies aiming for protection of the fragile subterranean ecosystems.
We are grateful to Mary Andriani, native speaker, for revision of the English style.