- Email: [email protected]
Beetles
Chapter 14
Beetles Arnaud Faille State Museum of Natural History, Stuttgart, Germany
Introduction Beetles (order Coleoptera) are probably the most diverse group of living beings, with ca. 360,000 species described in two main suborders (Adephaga and Polyphaga), so far about a quarter of the World Biodiversity. It can be easily distinguished from all other insects by the presence of the modified front pair of wings which is hardened into elytra. It is also the main group of insects to have successfully colonized the subterranean environments. In 1831 the first cave Coleoptera was discovered—one of the most remarkable species in terms of morphological adaptations to subterranean life—in a cave of Slovenia (former Carniola) by the count Fr. von Hohenwart, and described the following year under the name Leptodirus hochenwarti F.J. Schmid 1832. Since then, many species were discovered, first in the caves of the Dinaric karst, United States, and French Pyrenees, then in various subterranean environments of the world, mainly but not only karstic (see, e.g., the diversity of cave beetles in lava tubes). The diversity of cave Coleoptera is huge, with numerous microendemic species, most of them known from a single or a few number of caves. The most important part of the biodiversity of cave beetles is represented by three families which underwent speciose radiations, one aquatic: Dytiscidae, and two terrestrial: Carabidae and Leiodidae.
Diversity Various families of beetles colonized the subterranean environments, but three main radiations largely dominate cave beetle diversity. Two are in the suborder Adephaga: Dytiscidae (aquatic) and Carabidae (terrestrial), which is by far the main group of Coleoptera in subterranean ecosystems, and one is in Polyphaga: the family Leiodidae, with the tribe Leptodirini gathering the highest number of species in subterranean environments.
Dytiscidae Diving beetle species are known from subterranean aquifers, occasionally found in wells, bores, springs, or from the interstitial of gravel river banks (hyporheic zone). The first stygobitic Dytiscidae, Siettitia balsetensis (Fig. 1D), was described by Abeille de Perrin in 1904 from a well in Southeastern France, but the family remains species-poor in hypogean waters of Palearctic and Nearctic, as well as in tropical areas, whereas it is highly diversified in subterranean aquifers of Australia, especially the tribe Hydroporini.
Carabidae Carabidae is the most diverse family of beetles occurring in subterranean environments. The tribe Trechini, with more than 2500 species described, is by far the most diverse underground. This tribe contains the most morphologically modified ground beetles in terms of cave adaptations, and gave rise to remarkable underground radiations in Europe, Asia, and North America. Other Carabidae ground beetles colonized subterranean environments. This is the case of the tribe Pterostichini, with various genera occurring underground, in particular the speciose subtribe Sphodrina, and the tribes Platynini (genera Rhadine, Speagonum, Jujiroa, etc.), Zuphiini (genera Coarazuphium from Brazil, Ildobates from Spain, etc.) (Fig. 1B), Clivinini (Guiodytes from China, Clivina subterranea from the Movile cave, Romania, Trogloclivina from New Britain, Papua New Guinea, Italodytes from Italy, which is the most troglomorphic scaritine), as well as the subfamily Paussinae (Itamus, Eustra) (Fig. 1C). The tribe Anillini is cosmopolitan and composed of tiny soil species, some of them found only in caves and considered as troglobitic. A lot of species 102
Encyclopedia of Caves. https://doi.org/10.1016/B978-0-12-814124-3.00014-5 Copyright © 2019 Elsevier Inc. All rights reserved.
Beetles Chapter 14
103
FIG. 1 Habitus of some cave beetles: (A) Aphaenops alberti Jeannel, France (Carabidae, Trechini). (B) Ildobates neboti Espan˜ol, Spain (Carabidae, Zuphiini). (C) Eustra saripaensis Deuve, Sulawesi (Carabidae, Paussinae). (D) Siettitia balsetensis Abeille de Perrin, France (Dytiscidae, Hydroporini). (E) Anthroherpon hoermanni (Apfelbeck), Bosnia (Leiodidae, Leptodirini). (F) Decumarellus sarbui Poggi, Romania (Staphylinidae, Pselaphinae). (G) Domene cantonsi Espan˜ol, Morocco (Staphylinidae, Paederinae).
were recently described from mining areas of Australia, some at a depth of up to 60 m, and challenge our understanding of the frontiers between cavernicolous and endogean species (Baehr and Main, 2016). Leiodidae. The main group of Leiodidae diversified underground is the tribe Leptodirini (former Bathysciinae), with more than 900 species in 240 genera. It is a Palearctic group, with most of the species occurring in the Western Palearctic; the group did not reach Northern Africa. It is especially speciose in Dinarid chain, where the most cave-adapted species are encountered (see, e.g., Leptodirus, Anthroherpon (Fig. 1E)), Carpathian Mountains (with the three speciose genera Drimeotus, Pholeuon, and Sophrochaeta dominating) and Pyreneo-Cantabrian area (genera Speonomus, Quaestus, etc.). Most of the species are blind, apterous and depigmented. The second tribe in terms of number of cave species is the Ptomaphagini, with the widespread genus Ptomaphagus, frequent in the caves of North America and Asia (Peck, 1973). Some species of Ptomaphagini are microphthalmic, but all the species have eyes, except two: Ptomaphagus troglodytes Blas & Vives from Spain and Ptomaphaginus troglodytes Perreau & Ru˚zˇicˇka, just described from China. A unique cave Catopocerinae, the remarkable Glacicavicola bathyscioides Westcott occurs in North America, in lava tube ice caves of Idaho and Wyoming. Although much less diverse underground, other families of beetles occur in subterranean ecosystems. The main ones are the Staphylinidae with more than 200 species, most of them belonging to Pselaphinae (ca. 170 species, Fig. 1F), Paederinae and
104
Encyclopedia of Caves
Aleocharinae (Fig. 1G) and a few Scydmaeninae, Curculionidae (most of the species considered as soil dwellers), Histeridae, Noteridae (family of beetles with some stygobitic species (genus Phreatodytes) occurring in Japan, and Sulawesi (Speonoterus), a few species of Tenebrionidae. Various other families are frequently found underground, with many species living on bat guano, especially in tropical caves. None of those species display morphological adaptations to subterranean environment.
Morphology As most of the cave animals, subterranean beetles are remarkable by their convergent morphology, the “troglomorphies” or “troglobiomorphies” depending on authors, hiding their phylogenetic relationships (Fig. 1): increase in appendage length, anophthalmy or eye reduction, loss of pigmentation, softening of the exoskeleton, reduction in metathoracic wings and often presence of long sensory setae. The increase in antennae length is often correlated with an increase in the number of olfactory receptors. In stygobitic beetles, hypogean life is usually associated with a strong constriction between the pronotum and elytra, contrasting with the oval body shape of most of epigean species. In some Leptodirini, a remarkable swelling of the posterior part of the body is observed that causes the so-called “false physogastry”, as it only concerns elytra, forming an air chamber whereas abdomen remains flat. Cave beetles have a variety of shapes, but they were often assigned to various morphological types. The less modified types, including various genera and species, are characterized by stocky body shape and short legs and antennae. This is anophthalmous type for Carabidae, and bathyscioid type in Leiodidae. The species sharing the most remarkable adaptations to subterranean life (very long legs and antennae, slender body) were included in other morphological types: the aphaenopsian type for ground beetles (named after the genus Aphaenops from Pyrenean chain (Fig. 1A)) and the three facies pholeuonoid, leptodiroid, and scaphoid, for the slender species of Leptodirini, with a different combination of body outlines and shape of elytra ( Jeannel, 1943). Recent molecular data clearly state that these morphological types reflect more the diversity of ecology and adaptations of species than a phylogenetic signal. Eye and wing reduction and depigmentation are shared by cave and endogean fauna and sometimes challenging the ecological classification of beetles in some groups, for which the frontier between soil and cave is difficult to establish. All these convergent morphological characters obscure the real relationships between taxa, and challenge the understanding of the history of the cave beetles. As for other cave groups, the use of molecular tools allow a critical examination of the previous hypotheses based on morphology and is drawing a new vision of the phylogenies and scenarios that led to the present-day diversity of cave beetles.
Distribution Subterranean beetles occur on all continents except Antarctica; they also occur on some islands. The distribution pattern is unbalanced between groups, most of the terrestrial biodiversity of cave ground beetles occurring in Western Palearctic (Pyrenees, Cantabrian Chain, Alps, Dinarids), Southeastern China, Japan, North America, and New Zealand, whereas most of the diversity of Leiodidae Leptodirini is limited to Western Palearctic. The Dytiscidae are exceptionally diverse in Central Australia. Cave Carabidae are present on all continents except Antarctica. The most remarkable group in terms of troglomorphic features and specific diversity is the tribe Trechini. The tribe is distributed worldwide, but there are only a few hotspots with remarkable subterranean radiations. This is the case of Southeastern China (Sinaphaenops, Dongodytes, Giraffaphaenops, etc.) (Tian et al., 2016), Dinarid karst (Adriaphaenops, Anophthalmus, Neotrechus, etc.), Pyrenees (Aphaenops), Alps (Orotrechus, Italaphaenops, etc.), and Asturian chain (Apoduvalius). Trechini are also diversified in Eastern Caucasus, with remarkable genera of cave species (Meganophthalmus, Jeannelius, etc.), in Appalachian area (Pseudanophthalmus) (Barr, 1985), in Japan (Trechiama, Kurasawatrechus, etc.), in Carpathians (Duvalius). A few cave-adapted genera occur in other countries like Algeria, Turkey, Burma, Laos, Vietnam, Mexico, Guatemala, New Zealand, Tasmania, etc. Limestone caves of Central Texas (Balcones Escarpment and Edwards Plateau) are the scene of a remarkable subterranean radiation of the Rhadine Platynini ground beetles (Go´mez et al., 2016). Leiodidae Leptodirini is a Western Palearctic group, mostly diversified in Europe, with a few species reaching China (Sinobathyscia Perreau). The main cave radiations occur in Pyreneo-cantabrian area, Alps, and Balkans (Fresneda et al., 2011). Balkans (Dinarid Alps, Rhodopes, and Carpathians included) is the hottest spot of biodiversity of the group, with 369 species recorded so far. The group is here extremely diverse in shapes, and has the most troglomorphic species of the world (e.g., genera Anthroherpon, Leptodirus, Hadesia). Most of the diversity of stygobitic beetles belong to Dytiscidae and occur in Australian region with the majority of species and remarkable radiations occurring in calcrete aquifers of the Yilgarn Craton of Central Western Australia and Ngalia basin (Leys et al., 2003). Contrary to the two main terrestrial group of cave beetles, Dytiscidae are much less diversified in the Nearctic and Palearctic area.
Beetles Chapter 14
105
Disjunct distributions, and relictual status of cave coleoptera For a long time, cave beetles were considered as “living fossils”, and the subterranean colonization as a “dead end” ( Jeannel, 1943). In fact, there are numerous examples of species and genera of cave beetles which are the only representatives of groups especially diversified in other geographical areas of the world. This is the case for the Iberian cave species Dalyat mirabilis Mateu, unique representative of the tribe Dalyatini. Dalyat is a cave monospecific genus endemic from Southeastern Spain, the only European representative of a group known from Western North America and South Africa only (Carabidae Promecognathinae). A molecular study of the group concluded at a vicariant origin of Promecognathinae leading to Dalyat because of the isolation of the Iberian plate from Pangea in the late Jurassic to early Cretaceous (Ribera et al., 2005). Another example is the alpine genus of hypogean ground beetles Doderotrechus, related to high-altitude epigean Trechus from Himalaya. Other species-poor genera of cave beetles are isolated without any epigean representatives in the area. This is the case of the genera Horologion (Carabidae) and Glacicavicola (Leiodidae) in North America, the enigmatic subtribe of ground beetles Lovriciina from Croatia and Bulgaria, the cave Pselaphinae Decumarellus sarbui Poggi from Movile cave, the cave Platynini ground beetle Galiciotyphlotes from Spain, among many others. But some groups of cave beetles gave rise to flourishing hypogean lineages, contradicting the fact that cave evolution is a dead end. This is the case for various genera of diving beetles (Australian Hydroporini), ground beetles (Trechini of the genera Aphaenops in Pyrenees, Pseudanophthalmus in Appalachian mountains, Dongodytes in Guangxi, among others), and Leptodirini (Anthroherpon in Dinarid Alps, Drimeotus in Carpathians, Speonomus in Pyrenean chain, etc.) Anyway, the limited capacity for dispersal of cave beetles make them an excellent model for studying impact of past and predicted climatic changes on biodiversity (Sa´nchez-Ferna´ndez et al., 2016) or for the studies of historical biogeography, as their distribution is often better explained by the paleogeography of the area where they occur than by the distribution of the present-day epigean relatives.
Ecology Terrestrial cave beetles are usually restricted to underground environments with stable ecological conditions, dark zones with constant humidity, and stable temperature. Relative humidity close to saturation is the most important ecological parameter determining the presence of cave beetles, as softening of the exoskeleton makes cave beetles unable to avoid the loss of body water in dry conditions. Most of the diversity of cave beetles occurs in limestone areas, but numerous species colonized noncalcareous caves, especially lava tubes. Cave beetles are not restricted to caves, but occur in all the empty voids of the massifs, from the milieu souterrain superficiel (MSS) and cracks to the caves, with often some ecological preferences inside the karst explaining the rarity of some species in caves, whereas some of them can be common in MSS (Giachino and Vailati, 2010) (Fig. 2). In caves, they are often found on wet clay, stalagmites, under stones and close to accumulation of organic matter, rotten wood, etc. Some species can also be more common under stones at the entrance of the caves, or even far from the cave, if the humidity conditions are favorable. Carabidae and Dytiscidae are predaceous. Some guanobitic species of ground beetles hunt their preys on bat or bird guano. Some species were studied in detail and were found to be opportunist (Gers, 1995), but other are specialized on a type of prey (Kane and Poulson, 1976). Most of the Leptodirini are saprophagous, but some species developed remarkable adaptations like the hygropetricolous filter feeders in the genera Hadesia from Dinaric karst and Cansiliella from Italy, which are semiaquatic, and feed in flowing water and moonmilk.
Life cycle As the other cave animals, cave beetles are K-strategists: they are characterized by a long life span and the production of fewer progeny. Although hundreds of species of subterranean Coleoptera were described so far, very few is known regarding the first instars of most of the species. The only studies on the life cycles of cave beetles were carried out by Deleurance, who bred representative species from Leptodirini and Trechini in Moulis Cave (French Pyrenees). She found that in the most highly specialized subterranean species of Leptodirini, the female lays only a single huge egg—as it is the case for ground beetles (Fig. 3). The larva hatches and pupates directly without feeding or molting. For the less specialized Leptodirini, the contraction of the life cycle is intermediate between this extreme and a epigean life cycle: the larva still feeds, but the number of larval instars are lower than in epigean species (Deleurance, 1958). Deleurance suggested a similar evolution in ground beetles; this was supported by a recent study of ovaries of various species of epigean, endogean, and troglobitic Trechini, showing a drastic reduction in the number of ovarioles in cave species of Trechini (Faille and Pluot-Sigwalt, 2015).
106
Encyclopedia of Caves
FIG. 2 Distribution of trechine ground beetles inside the karst. (Modified from Juberthie C., Delay B., and M. Bouillon., 1980. Extension du milieu souterrain en zone non-calcaire: description d’un nouveau milieu et de son peuplement par les Col eopte`res troglobies. M em. Biosp eologie 7, 19–52.)
An active larva is known for some highly modified cave Trechini, but in radiations like Pyrenean Leptodirini or Trechini, contraction of the life cycle happened independently, and sometimes more than once in the history of the lineages. This contraction of the larval phase is correlated with an increase in diversification rate in Leptodirini (Cieslak et al., 2014).
Evolution and diversification Beetles are good candidates for studying the modalities of colonization of subterranean environments. Because of their strong ecological requirements, they are often located in one or a few karstic islands, and the gene flow between populations is extremely reduced or absent. This led to allopatric speciation and explains the high and narrow endemism of the subterranean beetles. Phylogeographic studies show a strong structuration between populations and geology, as is the case for the cave ground beetle Aphaenops cerberus (Fig. 4). Until recently the dating was mainly narrative; but calibrated phylogenies allow to date the main
FIG. 3 Aphaenops crypticola, oocyte. A gravid female with a mature oocyte in the right ovariole and the same oocyte in place within the female abdomen. Scale bar: 1 mm. (From Faille A., and D. Pluot-Sigwalt., 2015. Convergent evolution in the reduction of ovariole number associated with subterranean life in cave beetles. PLoS One 10 (7), e0131986.)
Beetles Chapter 14
107
FIG. 4 Fragmented distribution and haplotype network of the cave ground beetle A. cerberus (Dieck). Orange shaded: karstic areas. (Modified from Faille A., € Tanzler R., and E.F.A. Toussaint., 2015. On the way to speciation: shedding light on the karstic phylogeography of the micro-endemic cave beetle Aphaenops cerberus in the Pyrenees. J. Heredity 106 (6), 692–699). Picture: courtesy of Christian Vanderbergh, Used with permission.
diversifications events. The phylogenetical frameworks recently available for various groups of subterranean beetles allow the tracing of the evolution of troglomorphic characters and the recognition of key innovative features fostering the diversification of the groups. It allows us to identify how frequent the colonizations of subterranean environments occurred in the history of the groups, to date it, and to identify the paleogeographic and climatic events concomitant with these subterranean colonizations and the main splits in the phylogeny of the groups. The most common mode of speciation invoked for terrestrial and stygobitic beetles is allopatry, even for species occurring in sympatry (Guzik et al., 2011). The history of the Australian stygobitic Dytiscidae was studied using molecular tools, and the role of past climate on the subterranean colonization and subsequent diversification is recognized as key. Especially, phylogenies of the genus Paroster from the Yilgarn calcretes suggest a scenario of invasion of the subterranean medium by several surface dwelling ancestors during a period of aridification of the Miocene, from 10 to 5 millions years ago. The modality of speciation is debated, intra-calcrete speciation in sympatry is considered as a potential result of ecological-niche partitioning or intracalcrete speciation through micro-allopatric processes (Guzik et al., 2011). Nevertheless, colonization of subterranean waters occurred multiple times in the world; at least three independent colonizations of subterranean waters have been identified for North American dytiscids. The two main groups of terrestrial cave beetles were also studied in a phylogenetical framework using molecular tools (see, e.g., Faille et al., 2013; Ribera et al., 2010). Calibrated phylogenies were obtained for the two main clades of Western Palearctic cave beetles, Trechini and Leptodirini. It showed the monophyly of pyrenean hypogean Trechini, suggesting a single event of subterranean colonization with a secondary diversification of the group underground. In Alps, the pattern is more complex, with multiple subterranean colonizations, some of them recent (Duvalius clade: late Miocene origin), others much older suggesting a diversification posterior to the subterranean colonization and dated from the late Eocene-early Oligocene, as it is the case for the most modified cave Trechini of the Dinaro-Alpine area. The calibrated phylogeny of Western Mediterranean Leptodirini suggest that the colonization of subterranean Pyrenees began soon after Oligocene, whereas the currently recognized genera can be dated to the Late Oligocene-Miocene (Ribera et al., 2010). The nearctic hypogean diversification of Rhadine ground beetles is dated from the Late Miocene to early Pliocene (4–5My BP), and was said to be contemporary of the formation of the caves in the area (Go´mez et al., 2016). Most of the phylogenetic works on cave beetles found an early diversification of the main clades, always predating Pleistocene Last Glacial Maximum. The possibility of range expansion during narrow temporal windows was identified for the Pyrenean Leptodirini genus Troglocharinus, although the physical characteristic of the substratum appeared as a determinant of dispersal and gene flow (Rizzo et al., 2013).
108
Encyclopedia of Caves
In contrast with these flourishing radiations of subterranean beetles, phylogenetically and geographically isolated taxa and species-poor genera are common in cave beetles and their relictual status of more widespread faunas is doubtless.
Conservation Due to their microendemism, high species diversity, strong ecological requirement, and sometimes relictual status, cave beetles may deserve particular attention in terms of conservation. Most species of troglomorphic beetles have very narrow distributions and are often known from a single cave. As other species of cave animals, they are therefore very sensitive to local disturbances, especially destruction of karst by mining or quarrying activities, urbanization and development, pollution of subterranean waters and overpumping of aquifers. Regarding recreative activities, the impact of human disturbance on cave populations is variable, and depends mostly on the intensity of the perturbations and the characteristic of the caves; it has therefore to be considered on a case-by-case basis, and as far as possible, a monitoring has to be done before and during the activities (e.g., touristic exploitation), in order to test the impact and changes in the population of cave beetles. One of the main challenges of the future researches on cave beetles will be to describe all these discreet species and precise their distributions, as well as identify the threats in order to efficiently protect this remarkable biodiversity.
Bibliography Baehr, M., Main, D., 2016. New genera and species of subterranean Anilline Bembidiini from the Pilbara, northwestern Australia (Insecta: Coleoptera: Carabidae: Bembidiini: Anillina). Rec. W. Aust. Museum 31 (2), 59–89. Barr, T.C., 1985. Pattern and process in speciation of trechine beetles in eastern North America (Coleoptera: Carabidae: Trechinae). In: Ball, G.E. (Ed.), Taxonomy, Phylogeny, and Biogeography of Beetles and Ants. In: Series Entomologia 33, Dr. W. Junk Publishers, Dordrecht, The Netherlands, pp. 350–407. Cieslak, A., Fresneda, J., Ribera, I., 2014. Life history evolution and diversification in Leptodirini cave beetles. Proc. R. Soc. B Biol. Sci. 281, 20132978. Deleurance, S., 1958. La contraction du cycle evolutif des Coleopte`res Bathysciinae et Trechinae en milieu souterrain. Compt. Rend. Acad. Sci. 247, 752–753. Faille, A., Pluot-Sigwalt, D., 2015. Convergent evolution in the reduction of ovariole number associated with subterranean life in cave beetles. PLoS One 10 (7), e0131986. Faille, A., Casale, A., Balke, M., Ribera, I., 2013. A molecular phylogeny of alpine subterranean Trechini (Coleoptera: Carabidae). BMC Evol. Biol. 13, 248. Faille, A., T€anzler, R., Toussaint, E.F.A., 2015. On the way to speciation: shedding light on the karstic phylogeography of the micro-endemic cave beetle Aphaenops cerberus in the Pyrenees. J. Heredity 106 (6), 692–699. Fresneda, J., Grebennikov, V.V., Ribera, I., 2011. The phylogenetic and geographic limits of Leptodirini (Insecta: Coleoptera: Leiodidae: Cholevinae), with a description of Sciaphyes shestakovi sp. n. From the Russian Far East. Arthropod Syst. Phylog. 69 (2), 99–123. Gers, C., 1995. Strategie alimentaire de coleopte`res troglobies du genre Aphaenops (Coleoptera, Trechinae). Mem. Biospeologie 22, 35–45. Giachino, P.M., Vailati, D., 2010. The Subterranean Environment. Hypogean Life, Concepts and Collecting Techniques. WBA Handbooks, Verona, Italy. Go´mez, R.A., Reddell, J., Will, K., Moore, W., 2016. Up high and down low: molecular systematics and insight into the diversification of the ground beetle genus Rhadine LeConte. Mol. Phylogenet. Evol. 98, 161–175. Guzik, M.T., Cooper, S.J.B., Humphreys, W.F., Ong, S., Kawakami, T., Austin, A.D., 2011. Evidence for population fragmentation within a subterranean aquatic habitat in the Western Australian desert. Heredity 107, 215–230. Jeannel, R., 1943. Les Fossiles Vivants des Cavernes. Gallimard, Paris, France. Juberthie, C., Delay, B., Bouillon, M., 1980. Extension du milieu souterrain en zone non-calcaire: description d’un nouveau milieu et de son peuplement par les Coleopte`res troglobies. Mem. Biospeologie 7, 19–52. Kane, T., Poulson, T.L., 1976. Foraging by cave beetles: spatial and temporal heterogeneity of prey. Ecology 57 (4), 793–800. Leys, R., Watts, C.H., Cooper, S.J., Humphreys, W.F., 2003. Evolution of subterranean diving beetles (Coleoptera: Dytiscidae: Hydroporini, Bidessini) in the arid zone of Australia. Evolution 57, 2819–2834. Peck, S.B., 1973. A systematic revision and the evolutionary biology of the Ptomaphagus (Adelops) beetles of North America (Coleoptera: Leiodidae: Catopinae) with emphasis on cave-inhabiting species. Bull. Mus. Comp. Zool. 145 (2), 29–162. Ribera, I., Mateu, J., Belles, X., 2005. Phylogenetic relationships of Dalyat mirabilis Mateu, 2002, with a revised molecular phylogeny of ground beetles (Coleoptera, Carabidae). J. Zool. Syst. Evol. Res. 43, 284–296. Ribera, I., Fresneda, J., Bucur, R., Izquierdo, A., Vogler, A.P., Salgado, J.M., Cieslak, A., 2010. Ancient origin of a Western Mediterranean radiation of subterranean beetles. BMC Evol. Biol. 10 (1), 29. Rizzo, V., Comas, J., Fadrique, F., Fresneda, J., Ribera, I., 2013. Early Pliocene range expansion of a clade of subterranean Pyrenean beetles. J. Biogeogr. 40, 1861–1873. Sa´nchez-Ferna´ndez, D., Rizzo, V., Cieslak, A., Faille, A., Fresneda, J., Ribera, I., 2016. Thermal niche estimators and the capability of poor dispersal species to cope with climate change. Sci. Rep. 6. Tian, M., Huang, S., Wang, X., Tang, M., 2016. Contributions to the knowledge of subterranean trechine beetles in southern China’s karsts: five new genera (Insecta, Coleoptera, Carabidae, Trechinae). ZooKeys 564, 121–156.
Beetles Arnaud Faille State Museum of Natural History, Stuttgart, Germany
Introduction Beetles (order Coleoptera) are probably the most diverse group of living beings, with ca. 360,000 species described in two main suborders (Adephaga and Polyphaga), so far about a quarter of the World Biodiversity. It can be easily distinguished from all other insects by the presence of the modified front pair of wings which is hardened into elytra. It is also the main group of insects to have successfully colonized the subterranean environments. In 1831 the first cave Coleoptera was discovered—one of the most remarkable species in terms of morphological adaptations to subterranean life—in a cave of Slovenia (former Carniola) by the count Fr. von Hohenwart, and described the following year under the name Leptodirus hochenwarti F.J. Schmid 1832. Since then, many species were discovered, first in the caves of the Dinaric karst, United States, and French Pyrenees, then in various subterranean environments of the world, mainly but not only karstic (see, e.g., the diversity of cave beetles in lava tubes). The diversity of cave Coleoptera is huge, with numerous microendemic species, most of them known from a single or a few number of caves. The most important part of the biodiversity of cave beetles is represented by three families which underwent speciose radiations, one aquatic: Dytiscidae, and two terrestrial: Carabidae and Leiodidae.
Diversity Various families of beetles colonized the subterranean environments, but three main radiations largely dominate cave beetle diversity. Two are in the suborder Adephaga: Dytiscidae (aquatic) and Carabidae (terrestrial), which is by far the main group of Coleoptera in subterranean ecosystems, and one is in Polyphaga: the family Leiodidae, with the tribe Leptodirini gathering the highest number of species in subterranean environments.
Dytiscidae Diving beetle species are known from subterranean aquifers, occasionally found in wells, bores, springs, or from the interstitial of gravel river banks (hyporheic zone). The first stygobitic Dytiscidae, Siettitia balsetensis (Fig. 1D), was described by Abeille de Perrin in 1904 from a well in Southeastern France, but the family remains species-poor in hypogean waters of Palearctic and Nearctic, as well as in tropical areas, whereas it is highly diversified in subterranean aquifers of Australia, especially the tribe Hydroporini.
Carabidae Carabidae is the most diverse family of beetles occurring in subterranean environments. The tribe Trechini, with more than 2500 species described, is by far the most diverse underground. This tribe contains the most morphologically modified ground beetles in terms of cave adaptations, and gave rise to remarkable underground radiations in Europe, Asia, and North America. Other Carabidae ground beetles colonized subterranean environments. This is the case of the tribe Pterostichini, with various genera occurring underground, in particular the speciose subtribe Sphodrina, and the tribes Platynini (genera Rhadine, Speagonum, Jujiroa, etc.), Zuphiini (genera Coarazuphium from Brazil, Ildobates from Spain, etc.) (Fig. 1B), Clivinini (Guiodytes from China, Clivina subterranea from the Movile cave, Romania, Trogloclivina from New Britain, Papua New Guinea, Italodytes from Italy, which is the most troglomorphic scaritine), as well as the subfamily Paussinae (Itamus, Eustra) (Fig. 1C). The tribe Anillini is cosmopolitan and composed of tiny soil species, some of them found only in caves and considered as troglobitic. A lot of species 102
Encyclopedia of Caves. https://doi.org/10.1016/B978-0-12-814124-3.00014-5 Copyright © 2019 Elsevier Inc. All rights reserved.
Beetles Chapter 14
103
FIG. 1 Habitus of some cave beetles: (A) Aphaenops alberti Jeannel, France (Carabidae, Trechini). (B) Ildobates neboti Espan˜ol, Spain (Carabidae, Zuphiini). (C) Eustra saripaensis Deuve, Sulawesi (Carabidae, Paussinae). (D) Siettitia balsetensis Abeille de Perrin, France (Dytiscidae, Hydroporini). (E) Anthroherpon hoermanni (Apfelbeck), Bosnia (Leiodidae, Leptodirini). (F) Decumarellus sarbui Poggi, Romania (Staphylinidae, Pselaphinae). (G) Domene cantonsi Espan˜ol, Morocco (Staphylinidae, Paederinae).
were recently described from mining areas of Australia, some at a depth of up to 60 m, and challenge our understanding of the frontiers between cavernicolous and endogean species (Baehr and Main, 2016). Leiodidae. The main group of Leiodidae diversified underground is the tribe Leptodirini (former Bathysciinae), with more than 900 species in 240 genera. It is a Palearctic group, with most of the species occurring in the Western Palearctic; the group did not reach Northern Africa. It is especially speciose in Dinarid chain, where the most cave-adapted species are encountered (see, e.g., Leptodirus, Anthroherpon (Fig. 1E)), Carpathian Mountains (with the three speciose genera Drimeotus, Pholeuon, and Sophrochaeta dominating) and Pyreneo-Cantabrian area (genera Speonomus, Quaestus, etc.). Most of the species are blind, apterous and depigmented. The second tribe in terms of number of cave species is the Ptomaphagini, with the widespread genus Ptomaphagus, frequent in the caves of North America and Asia (Peck, 1973). Some species of Ptomaphagini are microphthalmic, but all the species have eyes, except two: Ptomaphagus troglodytes Blas & Vives from Spain and Ptomaphaginus troglodytes Perreau & Ru˚zˇicˇka, just described from China. A unique cave Catopocerinae, the remarkable Glacicavicola bathyscioides Westcott occurs in North America, in lava tube ice caves of Idaho and Wyoming. Although much less diverse underground, other families of beetles occur in subterranean ecosystems. The main ones are the Staphylinidae with more than 200 species, most of them belonging to Pselaphinae (ca. 170 species, Fig. 1F), Paederinae and
104
Encyclopedia of Caves
Aleocharinae (Fig. 1G) and a few Scydmaeninae, Curculionidae (most of the species considered as soil dwellers), Histeridae, Noteridae (family of beetles with some stygobitic species (genus Phreatodytes) occurring in Japan, and Sulawesi (Speonoterus), a few species of Tenebrionidae. Various other families are frequently found underground, with many species living on bat guano, especially in tropical caves. None of those species display morphological adaptations to subterranean environment.
Morphology As most of the cave animals, subterranean beetles are remarkable by their convergent morphology, the “troglomorphies” or “troglobiomorphies” depending on authors, hiding their phylogenetic relationships (Fig. 1): increase in appendage length, anophthalmy or eye reduction, loss of pigmentation, softening of the exoskeleton, reduction in metathoracic wings and often presence of long sensory setae. The increase in antennae length is often correlated with an increase in the number of olfactory receptors. In stygobitic beetles, hypogean life is usually associated with a strong constriction between the pronotum and elytra, contrasting with the oval body shape of most of epigean species. In some Leptodirini, a remarkable swelling of the posterior part of the body is observed that causes the so-called “false physogastry”, as it only concerns elytra, forming an air chamber whereas abdomen remains flat. Cave beetles have a variety of shapes, but they were often assigned to various morphological types. The less modified types, including various genera and species, are characterized by stocky body shape and short legs and antennae. This is anophthalmous type for Carabidae, and bathyscioid type in Leiodidae. The species sharing the most remarkable adaptations to subterranean life (very long legs and antennae, slender body) were included in other morphological types: the aphaenopsian type for ground beetles (named after the genus Aphaenops from Pyrenean chain (Fig. 1A)) and the three facies pholeuonoid, leptodiroid, and scaphoid, for the slender species of Leptodirini, with a different combination of body outlines and shape of elytra ( Jeannel, 1943). Recent molecular data clearly state that these morphological types reflect more the diversity of ecology and adaptations of species than a phylogenetic signal. Eye and wing reduction and depigmentation are shared by cave and endogean fauna and sometimes challenging the ecological classification of beetles in some groups, for which the frontier between soil and cave is difficult to establish. All these convergent morphological characters obscure the real relationships between taxa, and challenge the understanding of the history of the cave beetles. As for other cave groups, the use of molecular tools allow a critical examination of the previous hypotheses based on morphology and is drawing a new vision of the phylogenies and scenarios that led to the present-day diversity of cave beetles.
Distribution Subterranean beetles occur on all continents except Antarctica; they also occur on some islands. The distribution pattern is unbalanced between groups, most of the terrestrial biodiversity of cave ground beetles occurring in Western Palearctic (Pyrenees, Cantabrian Chain, Alps, Dinarids), Southeastern China, Japan, North America, and New Zealand, whereas most of the diversity of Leiodidae Leptodirini is limited to Western Palearctic. The Dytiscidae are exceptionally diverse in Central Australia. Cave Carabidae are present on all continents except Antarctica. The most remarkable group in terms of troglomorphic features and specific diversity is the tribe Trechini. The tribe is distributed worldwide, but there are only a few hotspots with remarkable subterranean radiations. This is the case of Southeastern China (Sinaphaenops, Dongodytes, Giraffaphaenops, etc.) (Tian et al., 2016), Dinarid karst (Adriaphaenops, Anophthalmus, Neotrechus, etc.), Pyrenees (Aphaenops), Alps (Orotrechus, Italaphaenops, etc.), and Asturian chain (Apoduvalius). Trechini are also diversified in Eastern Caucasus, with remarkable genera of cave species (Meganophthalmus, Jeannelius, etc.), in Appalachian area (Pseudanophthalmus) (Barr, 1985), in Japan (Trechiama, Kurasawatrechus, etc.), in Carpathians (Duvalius). A few cave-adapted genera occur in other countries like Algeria, Turkey, Burma, Laos, Vietnam, Mexico, Guatemala, New Zealand, Tasmania, etc. Limestone caves of Central Texas (Balcones Escarpment and Edwards Plateau) are the scene of a remarkable subterranean radiation of the Rhadine Platynini ground beetles (Go´mez et al., 2016). Leiodidae Leptodirini is a Western Palearctic group, mostly diversified in Europe, with a few species reaching China (Sinobathyscia Perreau). The main cave radiations occur in Pyreneo-cantabrian area, Alps, and Balkans (Fresneda et al., 2011). Balkans (Dinarid Alps, Rhodopes, and Carpathians included) is the hottest spot of biodiversity of the group, with 369 species recorded so far. The group is here extremely diverse in shapes, and has the most troglomorphic species of the world (e.g., genera Anthroherpon, Leptodirus, Hadesia). Most of the diversity of stygobitic beetles belong to Dytiscidae and occur in Australian region with the majority of species and remarkable radiations occurring in calcrete aquifers of the Yilgarn Craton of Central Western Australia and Ngalia basin (Leys et al., 2003). Contrary to the two main terrestrial group of cave beetles, Dytiscidae are much less diversified in the Nearctic and Palearctic area.
Beetles Chapter 14
105
Disjunct distributions, and relictual status of cave coleoptera For a long time, cave beetles were considered as “living fossils”, and the subterranean colonization as a “dead end” ( Jeannel, 1943). In fact, there are numerous examples of species and genera of cave beetles which are the only representatives of groups especially diversified in other geographical areas of the world. This is the case for the Iberian cave species Dalyat mirabilis Mateu, unique representative of the tribe Dalyatini. Dalyat is a cave monospecific genus endemic from Southeastern Spain, the only European representative of a group known from Western North America and South Africa only (Carabidae Promecognathinae). A molecular study of the group concluded at a vicariant origin of Promecognathinae leading to Dalyat because of the isolation of the Iberian plate from Pangea in the late Jurassic to early Cretaceous (Ribera et al., 2005). Another example is the alpine genus of hypogean ground beetles Doderotrechus, related to high-altitude epigean Trechus from Himalaya. Other species-poor genera of cave beetles are isolated without any epigean representatives in the area. This is the case of the genera Horologion (Carabidae) and Glacicavicola (Leiodidae) in North America, the enigmatic subtribe of ground beetles Lovriciina from Croatia and Bulgaria, the cave Pselaphinae Decumarellus sarbui Poggi from Movile cave, the cave Platynini ground beetle Galiciotyphlotes from Spain, among many others. But some groups of cave beetles gave rise to flourishing hypogean lineages, contradicting the fact that cave evolution is a dead end. This is the case for various genera of diving beetles (Australian Hydroporini), ground beetles (Trechini of the genera Aphaenops in Pyrenees, Pseudanophthalmus in Appalachian mountains, Dongodytes in Guangxi, among others), and Leptodirini (Anthroherpon in Dinarid Alps, Drimeotus in Carpathians, Speonomus in Pyrenean chain, etc.) Anyway, the limited capacity for dispersal of cave beetles make them an excellent model for studying impact of past and predicted climatic changes on biodiversity (Sa´nchez-Ferna´ndez et al., 2016) or for the studies of historical biogeography, as their distribution is often better explained by the paleogeography of the area where they occur than by the distribution of the present-day epigean relatives.
Ecology Terrestrial cave beetles are usually restricted to underground environments with stable ecological conditions, dark zones with constant humidity, and stable temperature. Relative humidity close to saturation is the most important ecological parameter determining the presence of cave beetles, as softening of the exoskeleton makes cave beetles unable to avoid the loss of body water in dry conditions. Most of the diversity of cave beetles occurs in limestone areas, but numerous species colonized noncalcareous caves, especially lava tubes. Cave beetles are not restricted to caves, but occur in all the empty voids of the massifs, from the milieu souterrain superficiel (MSS) and cracks to the caves, with often some ecological preferences inside the karst explaining the rarity of some species in caves, whereas some of them can be common in MSS (Giachino and Vailati, 2010) (Fig. 2). In caves, they are often found on wet clay, stalagmites, under stones and close to accumulation of organic matter, rotten wood, etc. Some species can also be more common under stones at the entrance of the caves, or even far from the cave, if the humidity conditions are favorable. Carabidae and Dytiscidae are predaceous. Some guanobitic species of ground beetles hunt their preys on bat or bird guano. Some species were studied in detail and were found to be opportunist (Gers, 1995), but other are specialized on a type of prey (Kane and Poulson, 1976). Most of the Leptodirini are saprophagous, but some species developed remarkable adaptations like the hygropetricolous filter feeders in the genera Hadesia from Dinaric karst and Cansiliella from Italy, which are semiaquatic, and feed in flowing water and moonmilk.
Life cycle As the other cave animals, cave beetles are K-strategists: they are characterized by a long life span and the production of fewer progeny. Although hundreds of species of subterranean Coleoptera were described so far, very few is known regarding the first instars of most of the species. The only studies on the life cycles of cave beetles were carried out by Deleurance, who bred representative species from Leptodirini and Trechini in Moulis Cave (French Pyrenees). She found that in the most highly specialized subterranean species of Leptodirini, the female lays only a single huge egg—as it is the case for ground beetles (Fig. 3). The larva hatches and pupates directly without feeding or molting. For the less specialized Leptodirini, the contraction of the life cycle is intermediate between this extreme and a epigean life cycle: the larva still feeds, but the number of larval instars are lower than in epigean species (Deleurance, 1958). Deleurance suggested a similar evolution in ground beetles; this was supported by a recent study of ovaries of various species of epigean, endogean, and troglobitic Trechini, showing a drastic reduction in the number of ovarioles in cave species of Trechini (Faille and Pluot-Sigwalt, 2015).
106
Encyclopedia of Caves
FIG. 2 Distribution of trechine ground beetles inside the karst. (Modified from Juberthie C., Delay B., and M. Bouillon., 1980. Extension du milieu souterrain en zone non-calcaire: description d’un nouveau milieu et de son peuplement par les Col eopte`res troglobies. M em. Biosp eologie 7, 19–52.)
An active larva is known for some highly modified cave Trechini, but in radiations like Pyrenean Leptodirini or Trechini, contraction of the life cycle happened independently, and sometimes more than once in the history of the lineages. This contraction of the larval phase is correlated with an increase in diversification rate in Leptodirini (Cieslak et al., 2014).
Evolution and diversification Beetles are good candidates for studying the modalities of colonization of subterranean environments. Because of their strong ecological requirements, they are often located in one or a few karstic islands, and the gene flow between populations is extremely reduced or absent. This led to allopatric speciation and explains the high and narrow endemism of the subterranean beetles. Phylogeographic studies show a strong structuration between populations and geology, as is the case for the cave ground beetle Aphaenops cerberus (Fig. 4). Until recently the dating was mainly narrative; but calibrated phylogenies allow to date the main
FIG. 3 Aphaenops crypticola, oocyte. A gravid female with a mature oocyte in the right ovariole and the same oocyte in place within the female abdomen. Scale bar: 1 mm. (From Faille A., and D. Pluot-Sigwalt., 2015. Convergent evolution in the reduction of ovariole number associated with subterranean life in cave beetles. PLoS One 10 (7), e0131986.)
Beetles Chapter 14
107
FIG. 4 Fragmented distribution and haplotype network of the cave ground beetle A. cerberus (Dieck). Orange shaded: karstic areas. (Modified from Faille A., € Tanzler R., and E.F.A. Toussaint., 2015. On the way to speciation: shedding light on the karstic phylogeography of the micro-endemic cave beetle Aphaenops cerberus in the Pyrenees. J. Heredity 106 (6), 692–699). Picture: courtesy of Christian Vanderbergh, Used with permission.
diversifications events. The phylogenetical frameworks recently available for various groups of subterranean beetles allow the tracing of the evolution of troglomorphic characters and the recognition of key innovative features fostering the diversification of the groups. It allows us to identify how frequent the colonizations of subterranean environments occurred in the history of the groups, to date it, and to identify the paleogeographic and climatic events concomitant with these subterranean colonizations and the main splits in the phylogeny of the groups. The most common mode of speciation invoked for terrestrial and stygobitic beetles is allopatry, even for species occurring in sympatry (Guzik et al., 2011). The history of the Australian stygobitic Dytiscidae was studied using molecular tools, and the role of past climate on the subterranean colonization and subsequent diversification is recognized as key. Especially, phylogenies of the genus Paroster from the Yilgarn calcretes suggest a scenario of invasion of the subterranean medium by several surface dwelling ancestors during a period of aridification of the Miocene, from 10 to 5 millions years ago. The modality of speciation is debated, intra-calcrete speciation in sympatry is considered as a potential result of ecological-niche partitioning or intracalcrete speciation through micro-allopatric processes (Guzik et al., 2011). Nevertheless, colonization of subterranean waters occurred multiple times in the world; at least three independent colonizations of subterranean waters have been identified for North American dytiscids. The two main groups of terrestrial cave beetles were also studied in a phylogenetical framework using molecular tools (see, e.g., Faille et al., 2013; Ribera et al., 2010). Calibrated phylogenies were obtained for the two main clades of Western Palearctic cave beetles, Trechini and Leptodirini. It showed the monophyly of pyrenean hypogean Trechini, suggesting a single event of subterranean colonization with a secondary diversification of the group underground. In Alps, the pattern is more complex, with multiple subterranean colonizations, some of them recent (Duvalius clade: late Miocene origin), others much older suggesting a diversification posterior to the subterranean colonization and dated from the late Eocene-early Oligocene, as it is the case for the most modified cave Trechini of the Dinaro-Alpine area. The calibrated phylogeny of Western Mediterranean Leptodirini suggest that the colonization of subterranean Pyrenees began soon after Oligocene, whereas the currently recognized genera can be dated to the Late Oligocene-Miocene (Ribera et al., 2010). The nearctic hypogean diversification of Rhadine ground beetles is dated from the Late Miocene to early Pliocene (4–5My BP), and was said to be contemporary of the formation of the caves in the area (Go´mez et al., 2016). Most of the phylogenetic works on cave beetles found an early diversification of the main clades, always predating Pleistocene Last Glacial Maximum. The possibility of range expansion during narrow temporal windows was identified for the Pyrenean Leptodirini genus Troglocharinus, although the physical characteristic of the substratum appeared as a determinant of dispersal and gene flow (Rizzo et al., 2013).
108
Encyclopedia of Caves
In contrast with these flourishing radiations of subterranean beetles, phylogenetically and geographically isolated taxa and species-poor genera are common in cave beetles and their relictual status of more widespread faunas is doubtless.
Conservation Due to their microendemism, high species diversity, strong ecological requirement, and sometimes relictual status, cave beetles may deserve particular attention in terms of conservation. Most species of troglomorphic beetles have very narrow distributions and are often known from a single cave. As other species of cave animals, they are therefore very sensitive to local disturbances, especially destruction of karst by mining or quarrying activities, urbanization and development, pollution of subterranean waters and overpumping of aquifers. Regarding recreative activities, the impact of human disturbance on cave populations is variable, and depends mostly on the intensity of the perturbations and the characteristic of the caves; it has therefore to be considered on a case-by-case basis, and as far as possible, a monitoring has to be done before and during the activities (e.g., touristic exploitation), in order to test the impact and changes in the population of cave beetles. One of the main challenges of the future researches on cave beetles will be to describe all these discreet species and precise their distributions, as well as identify the threats in order to efficiently protect this remarkable biodiversity.
Bibliography Baehr, M., Main, D., 2016. New genera and species of subterranean Anilline Bembidiini from the Pilbara, northwestern Australia (Insecta: Coleoptera: Carabidae: Bembidiini: Anillina). Rec. W. Aust. Museum 31 (2), 59–89. Barr, T.C., 1985. Pattern and process in speciation of trechine beetles in eastern North America (Coleoptera: Carabidae: Trechinae). In: Ball, G.E. (Ed.), Taxonomy, Phylogeny, and Biogeography of Beetles and Ants. In: Series Entomologia 33, Dr. W. Junk Publishers, Dordrecht, The Netherlands, pp. 350–407. Cieslak, A., Fresneda, J., Ribera, I., 2014. Life history evolution and diversification in Leptodirini cave beetles. Proc. R. Soc. B Biol. Sci. 281, 20132978. Deleurance, S., 1958. La contraction du cycle evolutif des Coleopte`res Bathysciinae et Trechinae en milieu souterrain. Compt. Rend. Acad. Sci. 247, 752–753. Faille, A., Pluot-Sigwalt, D., 2015. Convergent evolution in the reduction of ovariole number associated with subterranean life in cave beetles. PLoS One 10 (7), e0131986. Faille, A., Casale, A., Balke, M., Ribera, I., 2013. A molecular phylogeny of alpine subterranean Trechini (Coleoptera: Carabidae). BMC Evol. Biol. 13, 248. Faille, A., T€anzler, R., Toussaint, E.F.A., 2015. On the way to speciation: shedding light on the karstic phylogeography of the micro-endemic cave beetle Aphaenops cerberus in the Pyrenees. J. Heredity 106 (6), 692–699. Fresneda, J., Grebennikov, V.V., Ribera, I., 2011. The phylogenetic and geographic limits of Leptodirini (Insecta: Coleoptera: Leiodidae: Cholevinae), with a description of Sciaphyes shestakovi sp. n. From the Russian Far East. Arthropod Syst. Phylog. 69 (2), 99–123. Gers, C., 1995. Strategie alimentaire de coleopte`res troglobies du genre Aphaenops (Coleoptera, Trechinae). Mem. Biospeologie 22, 35–45. Giachino, P.M., Vailati, D., 2010. The Subterranean Environment. Hypogean Life, Concepts and Collecting Techniques. WBA Handbooks, Verona, Italy. Go´mez, R.A., Reddell, J., Will, K., Moore, W., 2016. Up high and down low: molecular systematics and insight into the diversification of the ground beetle genus Rhadine LeConte. Mol. Phylogenet. Evol. 98, 161–175. Guzik, M.T., Cooper, S.J.B., Humphreys, W.F., Ong, S., Kawakami, T., Austin, A.D., 2011. Evidence for population fragmentation within a subterranean aquatic habitat in the Western Australian desert. Heredity 107, 215–230. Jeannel, R., 1943. Les Fossiles Vivants des Cavernes. Gallimard, Paris, France. Juberthie, C., Delay, B., Bouillon, M., 1980. Extension du milieu souterrain en zone non-calcaire: description d’un nouveau milieu et de son peuplement par les Coleopte`res troglobies. Mem. Biospeologie 7, 19–52. Kane, T., Poulson, T.L., 1976. Foraging by cave beetles: spatial and temporal heterogeneity of prey. Ecology 57 (4), 793–800. Leys, R., Watts, C.H., Cooper, S.J., Humphreys, W.F., 2003. Evolution of subterranean diving beetles (Coleoptera: Dytiscidae: Hydroporini, Bidessini) in the arid zone of Australia. Evolution 57, 2819–2834. Peck, S.B., 1973. A systematic revision and the evolutionary biology of the Ptomaphagus (Adelops) beetles of North America (Coleoptera: Leiodidae: Catopinae) with emphasis on cave-inhabiting species. Bull. Mus. Comp. Zool. 145 (2), 29–162. Ribera, I., Mateu, J., Belles, X., 2005. Phylogenetic relationships of Dalyat mirabilis Mateu, 2002, with a revised molecular phylogeny of ground beetles (Coleoptera, Carabidae). J. Zool. Syst. Evol. Res. 43, 284–296. Ribera, I., Fresneda, J., Bucur, R., Izquierdo, A., Vogler, A.P., Salgado, J.M., Cieslak, A., 2010. Ancient origin of a Western Mediterranean radiation of subterranean beetles. BMC Evol. Biol. 10 (1), 29. Rizzo, V., Comas, J., Fadrique, F., Fresneda, J., Ribera, I., 2013. Early Pliocene range expansion of a clade of subterranean Pyrenean beetles. J. Biogeogr. 40, 1861–1873. Sa´nchez-Ferna´ndez, D., Rizzo, V., Cieslak, A., Faille, A., Fresneda, J., Ribera, I., 2016. Thermal niche estimators and the capability of poor dispersal species to cope with climate change. Sci. Rep. 6. Tian, M., Huang, S., Wang, X., Tang, M., 2016. Contributions to the knowledge of subterranean trechine beetles in southern China’s karsts: five new genera (Insecta, Coleoptera, Carabidae, Trechinae). ZooKeys 564, 121–156.