Cave and Subterranean Ants

Attempting to classify nature is fraught with difficulty, and defining what is and isn't a "cave" ant is no exception. Nature seems to have a fondness for continua while humans prefer to place things in neat little boxes. This is certainly the case here. The end-points of the cave-ant/non-cave-ant continuum can be clearly defined and some species can be unambiguously assigned to these categories. However, many species fall between these end-points and their exact classification can, at times, be somewhat arbitrary. Nonetheless, it is useful to develop a classification framework, even if it is not always clearly applicable.

Boutin (2004) provides a detailed discussion of this problem and develops the following classification of cave-inhabiting taxa. He notes that these organisms live in a great variety of subterranean habitats and any reasonable classification of them must necessarily be based on ecological criteria that reflect the wide variety of habitats and life histories utilized. Several different classifications have been proposed, although they cannot always be easily compared because the authors frequently use similar names but employ different definitions.

Most speleobiologists recognize three different types of inhabitants: troglobites, troglophiles and trogloxenes.

Troglobites
Troglobites are species permanently and exclusively living in caves or other subterranean cavities such as that of the “superficial underground compartment” (also called MSS, mesovoid shallow substratum or milieu souterrain superficiel, a network of air-filled underground voids between the rock fragments found in scree (talus) deposits) (Camacho, 1992; Humphreys, 2000; Juberthie, 2000), or in fissures or interstices providing large spaces compared to the animal body size. They are sometimes considered as the true cave-dwelling organisms and are often called troglobites (Holsinger & Culver, 1988). The adjectives “troglobiontic” or “troglobitic” are used, but compound names including troglobite are generally preferred by many authors. Troglobites generally present troglomorphic (or “troglobiomorphic”) characteristics sensu Christiansen (1962), including morphological traits such as reduction or loss of eyes and tegument pigmentation, thinning of cuticle, and elongation of appendages, especially antennae, in arthropods. In addition, they frequently have biological, ecological, or behavioural traits such as a low metabolism and fecundity associated with a K-reproductive strategy, and a tendency to the loss of circadian and seasonal rhythms. This set of characteristics is called “troglomorphy” (or “troglobiomorphy”) and is considered an adaptation to subterranean environments. Troglobites exhibiting marked troglomorphic traits are generally considered as “paleotroglobites” as their ancestors colonized subterranean habitats in ancient times, from millions to hundreds of million years ago. When the ancestral group has disappeared from all surface habitats, the paleotroglobites, being the sole representative of the group, are often called “living fossils” or relict species. Other troglobites are genuinely limited to caves and differ from all closely related surface (epigean) species in respect to some specific traits but may exhibit few or no troglomorphic traits. These species are called “neotroglobites”, having relatively recently colonized the subterranean habitat. Conversely, some epigean organisms may appear to possess troglomorphic characteristics even though they do not inhabit subterranean environments.

Troglophiles
Troglophiles are species that can establish and maintain subterranean populations but also occur in surface habitats that may have little similarity with the cave environment. They are able to support viable reproductive hypogean populations and may be common in caves, but are not obligate subterranean inhabitants. They may exhibit only some troglomorphic traits but these are generally less marked than in troglobites. They often look very similar to closely related surface species. Sometimes their status is uncertain, such as when they are theoretically able to live in surface habitats but are unknown outside of caves.

Trogloxenes
Trogloxenes are species that sometimes occur in caves but belong to surface communities, usually living and feeding in epigean habitats. They have sometimes been called “xenocaval” and as some are found in caves only by chance they have also been called “tychocaval” organisms or “accidentals” (Holsinger & Culver, 1988). However, the term trogloxene is by far the most commonly used and following Racovitza (1907) it is usual to distinguish the “regular trogloxenes” (such as the bats that usually reside in caves but feed outside of the cave) and the accidental or “occasional trogloxenes”, corresponding to the tychocaval or accidentals, including many surface forms exceptionally and passively drawn into some caves (surface fishes or aquatic invertebrates) or temporarily resting in caves (snakes, birds, rodents, or many terrestrial invertebrates).

Troglomorphy
Assessing the troglobitic status of a taxon is not easy. However, troglomorphy (Christiansen, 1962; Boutin, 2004), i.e. the set of morphological traits characteristics of cave organisms, is always a strong indication of troglobitism {while the opposite is not always true). Troglobiomorphy in arthropods is defined by four morphological traits: loss of wings in winged arthropod groups, reduction of eyes, reduction of tegumentary pigment and elongation of appendages (Vandel, 1964; Christiansen, 1965; Culver, 1982; Marques and Gnaspini, 2001). All known specimens of Leptogenys khammouanensis are workers, which are always apterous in ants. We do not know therefore the state of the first character in this but the last three traits are present. See Roncin & Deharveng (2003) for further details.

Ants in Caves
Though frequently cited from caves, ants have not provided so far any unambiguously troglobitic species. Most records (Wilson, 1962; Tinaut and Lopez, 2001) concern in fact accidental occurrences, generally not far from cave entrance (Decu et al., 1998). Most species supposed to be strictly cavernicolous have been later found also outside caves. Even the rare Hypoponera ragusai considered by Tinaut (2001) to be limited to caves in Europe has been collected outside caves in France (Bernard, 1968) and in the Mediterranean islands of Lampedusa and Linosa (Mei, 1992, 1995).

This rarity of ants in caves concerns essentially temperate regions. Though limited, available evidence suggests that Formicidae might be much more frequent in tropical caves. More than sixty species have already been collected from the dark part of various caves of Southeast Asia (Roncin et al., 2001, and unpublished data). Most of these species, well-known outside, are represented by isolated specimens in cave collections. But several are regular guano inhabitants, like Hypoponera confinis in the Farm caves of Myanmar (Annandale et al., 1913) and an unidentified species in the Mulu caves of Sarawak (Chapman, 1982). In fact, ants were present in most guano caves recently sampled in Southeast Asia, with Hypoponera the dominant genus (Roncin et al., 2001 ). They were sometimes found very far from cave entrance, living in loose colonies, foraging in or around the guano piles, where they are believed to prey on a rich fauna of micro- and meso-arthropods. None of these regular guano species are troglobiomorphic, and all were also collected outside caves. Among the hundreds of caves prospected so far in all regions of Southeast Asia (see Juberthie and Decu, 2001 for an overview), troglobiomorphic species were found only in Laos with L. khammouanensis.

Having analysed what was known about cave ants, Wilson (1962) hypothesized that social insects “never become truly troglobitic” because “they are unable to maintain sufficiently large cave demes” (implicitly because of food scarcity). The well-known link between troglobiomorphy and oligotrophic habitats (Deharveng and Bedos, 2000) certainly explains the extreme difficulty for ants to establish long-term colonies and to adapt to cave environment. This view is challenged today by the discovery of L. khammouanensis with its clear troglobiomorphic morphology. The unusually large underground voids of Laos may have given the opportunity for such an evolution to take place, by providing large food reservoirs on the long-term. To confirm this exciting hypothesis, it remains to document the peculiarities of the biology and social life of the new species (Tinaut and Lopez, 2001).

Troglobiomorphic characters in Leptogenys - The genus Leptogenys has already been found in caves. Leptogenys jeanneli Santschi, 1914 was described from a cave in Tanzania, and Leptogenys diminuta (Smith, 1857) was collected in the Batu Caves of peninsular Malaysia (Wilson, 1962; McClure, 1965). However, none of these species is cave-restricted, and none exhibits the combination of troglobiomorphic traits of L. khammouanensis.

A group of Leptogenys processionalis sensu Taylor (1969) (=fallax-group of Andersen, 2000), which comprises three Australian species, Leptogenys fallax (Mayr, 1876), Leptogenys tricosa Taylor, 1969 and Leptogenys fortior Forel 1900, and the Oriental species Leptogenys myops (Emery, 1887), Leptogenys crassicornis Emery, 1895 and Leptogenys processionalis (Jerdon, 1851 ). Species of this group possess also light color and reduced eyes varying from a single (L. tricosa) to about fifteen facets, but antennae are short, and size is small. Such a morphology appears as a classical adaptation to endogeous, not to cave life. At least several African species in the guineensis- and the nitida-group also possess small eyes, and are yellow brown to dark brown. However their head and appendages are so not elongated.

Leptogenys khammouanensis was encountered far from the entrance in two big caves, Tham Nam Non (22 km long, the longest cave of continental Southeast Asia, Mouret, 2001) and Tham The (2.2 km long, Brouquisse, 1999). In spite of being 25 km apart and in different hydrogeological systems, both caves do belong to the same, uninterrupted, huge limestone unit. In Tham Nam Non, L. khammouanensis was collected at about 4.5 km of the entrance. These giant caves of the Khammouan karst host a rich troglobitic fauna, only recently discovered: microphthalmic crabs (Erebusa calobates, Yeo and Ng), various blind terrestrial lsopods, Araneids and Millipeds (Polydesmidae, Glomeridae), Campodeids, springtails, blind Nocticolid cockroaches, blind or microphthalmic Diestrammena sp. crickets (Besson et al., 2001 ). As numerous species of Leptogenys are woodlices-hunters (for a full list of references see: Holldobler and Wilson, 1990; Dejean 1997), the terrestrial isopods frequent in these caves could constitute a potential diet of L. khammouanensis, but this has to be confirmed.

In its slender habitus (very elongate head, mesosoma, petiole, antennae and legs), Leptogenys khammouanensis is similar to Leptogenys ergatogyna from Africa and to Leptogenys assamensis from Assam. But both species differ from L. khammouanensis by their black color and larger eyes, and cannot be considered as troglobiomorphic. No species of Leptogenys therefore approaches L. khammouanensis in its combination of troglobiomorphic characters.

Only one species of Formicidae associated with caves, Aphaenogaster cardenai, could be associated to subterranean habitats (Decu et al., 1998, Tinaut and Lopez, 2001). This rare Spanish species has always been collected in cryptic habitats: under big rocks, galleries of rodents and caves. However in this latter habitat no nests have ever been found, which led these authors to postulate that A. cardenai is more probably an inhabitant of the MSS (“Milieu Souterrain Superficial” of Juberthie et al. 1980, “superficial underground compartment” in Humphreys, 2000), than a strictly cave dwelling species.

A. cardenai is related to Aphaenogaster splendida and Aphaenogaster ovaticeps. All have reduced eyes, slender body, elongate appendages and often pale color, compared to other species of the genus. Bernard (1968: 136) stressed the peculiar morphology of the species then known and noted that they have “un facies aphaenopsien de cavernicole" (“an Aphaenops-like morphology of cave species”). He supposed they inhabit hypogean habitats, probably deep cracks that they rarely leave, hence their rarity in collection. However a few captures from surface habitats (Forel, 1911; Wheeler and Mann, 1916) could indicate nocturnal activity more than hypogean life.

Cave Ants
Few ants are known to reside permanently in caves (Pape, 2016) or exhibit troglomorphism (Christiansen 2005). Whereas Nylanderia pearsei from the Yucatán Peninsula and an undescribed Leptogenys species from central Texas are subterranean so far as is known (Wheeler 1938; Reddell 1977; Cokendolpher et al. 2009), neither is unambiguously troglomorphic in phenotype. Compelling arguments for troglomorphism among described ants have heretofore only been made for Leptogenys khammouanensis and Aphaenogaster gamagumayaa. When compared to their respective closest relatives, both display a gracile habitus, pale colouration and reduced compound eyes (Roncin and Deharveng 2003; Naka and Maruyama 2018). Additionally, L. khammouanensis was collected in two large calcareous caves in Laos, ranging from 500 m to several kilometres from the cave entrance (Roncin and Deharveng 2003), whereas A. gamagumayaa was collected ~20 m within a calcareous cave on Okinawa, apparently nesting in the floor of an aphotic guano hall (Naka and Maruyama 2018, pp. 138–139).