Troglomorphic Species Research Articles

A New Endogean, Dwarf, and Troglomorphic Species of Swamp Eel of the Genus Ophisternon (Synbranchiformes: Synbranchidae) from Costa Rica: Evidence from Comparative Mitogenomic and Anatomical Data

A New Endogean, Dwarf, and Troglomorphic Species of Swamp Eel of the Genus Ophisternon (Synbranchiformes: Synbranchidae) from Costa Rica: Evidence from Comparative Mitogenomic and Anatomical Data

Considerable gene flow in troglomorphic cockroach species across a vast subterranean landscape

AbstractAimThere has been growing interest in non‐cave subterranean habitats and their influence on the evolution of troglomorphic (i.e. ‘subterranean adapted’) species. Studies on the diversification of aquatic subterranean organisms in these habitats generally support the ‘subterranean island’ hypothesis, whereby isolated subterranean refuges lead to patterns of short‐range endemism. However, their terrestrial counterparts have received less attention. We aimed to elucidate the applicability of the ‘subterranean island’ hypothesis to terrestrial subterranean fauna through genetic analyses of two widespread troglomorphic cockroach species. To investigate the influence of subterranean biogeography, we also analysed a closely related species that inhabits ‘classic’ cave environments to represent a contrasting biogeographic comparison.LocationPilbara region, Western Australia, and the Chillagoe‐Mungana Caves, Queensland (Australia).TaxaCave cockroach species: Nocticola cockingi, Nocticola quartermainei and Nocticola australiensis.MethodsWe used DArTseq to generate genome‐wide SNPs in 78 samples, and Sanger sequencing to generate 16S mtDNA data. We then applied various population genomic analyses to characterize the distribution of genetic diversity within the three study species.ResultsWe identified distinct genetic clusters within the two Pilbara species; however, there appeared to be a notable lack of discernible population differentiation across large parts of their range (>135 km), opposing the subterranean island hypothesis. The highest level of population differentiation in the three study species was between the two caves in Queensland, ~3 km apart.Main ConclusionsThe Pilbara subterranean habitat appeared to be conducive to gene flow across relatively large distances, contrasting high levels of endemism observed in other subterranean taxa within the region. The disparate patterns of gene flow among the Pilbara and Queensland study species emphasize the significance of differing subterranean habitats on patterns of dispersal and vicariance. These inferences will inform conservation genetic management of these species, and may help elucidate the evolutionary paradox of widespread subterranean fauna.

Feihu Dong, a New Hotspot Cave of Subterranean Biodiversity from China

China is a country with abundant karst landscapes, but research on cave biodiversity is still limited. Currently, only Ganxiao Dong, located in Huanjiang, Guangxi, has been reported as a hotspot for cave biodiversity. Many of the world’s most troglomorphic species in the major groups of cave animals have been recently discovered in China, making the existence of many more hotspots in the country likely. Feihu Dong, one of these potential hotspot caves, has been systematically investigated to complement a preliminary species list of 1995, leading to the discovery of 62 species of animals from the cave. Among them, 27 are considered troglobionts or stygobionts, 26 are considered troglophiles or stygophiles, and nine are classified as trogloxenes or stygoxenes. Research on the cave biodiversity of Feihu Dong has demonstrated that it currently holds the highest number of known cave animal species in China. Among the most remarkable features of this fauna is the co-occurrence of five species of cave-obligate beetles, all modified for cave life. The biological survey was limited to a small part of the cave. Several habitats (like guano) have not been investigated so far, and several important cave groups have been insufficiently or not sampled (like Ostracoda). Meanwhile, the system increases in length with each new caving expedition. Further discoveries of cave organisms in Feihu Dong are therefore expected. As Feihu Dong and Ganxiao Dong are the only caves in China that have been extensively studied for a large range of organisms, and as they are located in karstic areas that are similar in richness to other regions of southern China, it can be confidently assumed that several other caves of high biodiversity will be discovered in the coming years.

The Água Clara Cave System in Northeastern Brazil: The Richest Hotspot of Subterranean Biodiversity in South America

The Água Clara Cave System (ACCS) in Brazil is the richest hotspot of subterranean biodiversity in South America. In this study, we present an updated list of cave-restricted species in the ACCS and compare it with previously published hotspots in Brazil. Our list of cave-obligate fauna comprises 31 species, including 23 troglobionts and 8 stygobionts. The exceptional diversity of the ACCS can be attributed to factors related to the high dispersal potential of cave fauna within the system, high surface productivity, and the large size of the cave system size. Notably, we observed highly troglomorphic species in the ACCS, some of which are the most troglomorphic species in their respective groups in Brazil. The huge volume of galleries, high humidity, and trophic conditions prevailing in the ACCS may have played a role in shaping the strong troglomorphic traits observed in these species. However, all the obligate cave species in the ACCS require conservation attention and are at an elevated risk of extinction due to their limited ranges, few occurrences, and many potential threats. This study sheds light on the biodiversity and conservation status of cave-restricted fauna in the ACCS and highlights the importance of protecting these unique ecosystems.

Spatial genetic structure of Dinaric cave-dwelling spiders

Caves put strong constraints on organisms living there, which results in acquisition of variety of troglomorphic traits, most obvious ones being depigmentation and degradation of visual system (Christiansen 2012). Cave habitats are considered fragmented, and the animals living there face limited connectivity between potential habitats (Barr 1967, Bregović and Zagmajster 2016, Trontelj 2018). Additionally, once adapted to underground conditions, cave-dwellers are thought to be unable to use the surface for dispersal, thus demonstrating population dynamics similar to those of the species found in islands (Barr and Holsinger 1985). We compared the population genetic structure of several cave spider species with different biology and ecology from different caves in the Dinarides. Namely, depigmented and anophthalmic Dysderidae species which were never collected outside caves, and several species from the genus Troglohyphantes, which exhibit different levels of troglomorphisms and dependency on cave habitat (some, like T. excavatus and T. kordunlikanus, can be occasionally found in surface habitats). Additionally, Dysderidae are wandering active hunters, while all Troglohyphantes species spin webs. In our study, we applied a hybridization-capture approach, i.e., HyRAD (Suchan et al. 2016) to extract and capture DNA from historical samples. We compared the population genetic structures among the species, and studied isolation by distance, and identified contrasted genetic structures related to the biology and ecology of each species. We identified a deeper population structuring and more pronounced patterns of isolation by distance in the highly troglomorphic species compared to the less troglomorphic ones. Species that can occasionally be found in surface habitats showed less structured populations compatible with higher dispersal ability. Additionally, we detected several common breaks in gene flow for most studied species, some of which can be explained by geographic and geologic features.

Recent speciation and phenotypic plasticity within a parthenogenetic lineage of levantine whip spiders (Chelicerata: Amblypygi: Charinidae)

Caves constitute ideal study systems for investigating adaptation and speciation, as the abiotic conditions shared by aphotic habitats exert a set of environmental filters on their communities. Arachnids constitute an important component of many cave ecosystems worldwide. We investigated the population genomics of two whip spider species: Sarax ioanniticus, a widely distributed parthenogenetic species found across the eastern Mediterranean; and S. israelensis, a recently described troglomorphic species that is endemic to caves in Israel. Here, we show that S. israelensis is completely genetically distinct from S. ioanniticus and most likely also a parthenogen. Counterintuitively, despite the lack of genetic variability within S. ioanniticus and S. israelensis, we discovered considerable variation in the degree of median eye reduction, particularly in the latter species. Natural history data from captive-bred specimens of S. israelensis validated the interpretation of parthenogenesis. Our results are most consistent with a scenario of a sexual ancestral species that underwent speciation, followed by independent transitions to apomictic parthenogenesis in each of the two daughter species. Moreover, the lack of genetic variability suggests that variation in eye morphology in S. israelensis is driven exclusively by epigenetic mechanisms.

Two new species of cave-adapted pseudoscorpions (Pseudoscorpiones, Chthoniidae) from Yunnan, China.

Two new cave-adapted pseudoscorpion species belonging to the family Chthoniidae are described: Tyrannochthoniuspandussp. nov. from Biyu Cave (Yunnan: Luxi) and Lagynochthoniuslaoxueyanensissp. nov. from Laoxueyan Cave (Yunnan: Yanshan). Both of them, collected from the dark zone of caves, are highly troglomorphic species.

Four new species of troglomorphic Coecobrya Yosii, 1956 (Collembola, Entomobryidae) from Thailand based on morphological and molecular evidence, with an updated key of Thai troglomorphic species

Four new species of troglomorphic Coecobrya Yosii, 1956 are described from caves located in the central and northeastern regions of Thailand. Coecobrya whittenisp. nov. and C. troglobiasp. nov. are from Khon Kaen province, C. ellisisp. nov. is from Phetchabun province and C. phitsanulokensissp. nov. is from Phitsanulok province. They all exhibit remarkable troglobitic characters i.e. elongated antennae, legs and furca, slender claw complex and large body size. Coecobrya whittenisp. nov. is similar to C. troglobiasp. nov. and they were found a distance of only 3.4 km from each other. However, they are mainly different in the number of An mac on dorsal head and number of chaetae of Th. II. Likewise, C. ellisisp. nov. is similar to C. phitsanulokensissp. nov.. However, they differ in the number of An mac on the dorsal head, the number of central mac on Abd. II, central mac on Abd. IV, lateral mac on Abd. IV and the number of inner teeth of the claw. Moreover, C. ellisisp. nov. has orange pigment dots on the body, a unique character, considering that all other troglomorphic Coecobrya species in Thailand are devoid of pigmentation. The results of the molecular approach based on two partial mitochondrial markers (COI and 16S rDNA) and a nuclear gene fragment (28S rDNA) supported the results of morphological species discrimination in separating the four nominal populations as valid species. An updated dichotomous key of Thai troglomorphic Coecobrya species is also given.

Ganxiao Dong: A Hotspot of Cave Biodiversity in Northern Guangxi, China

Located in the core zone of Mulun National Nature Reserve in northern Guangxi, the limestone cave Ganxiao Dong harbours the richest cave fauna currently known in China. In total, 26 species of cave invertebrates have been recognized so far, in spite of limited sampling efforts. Of them, 20 are troglobionts or stygobionts, including one snail, four millipedes, three spiders, one harvestman, three isopods, two springtails, two crickets, one non-glowing sticky worm, and three trechine beetles. Six other species are troglophiles. The most remarkable characteristic of this fauna is its high number of troglomorphic species, especially among millipedes, crickets and beetles.

Five million years in the darkness: A new troglomorphic species of Cryptops Leach, 1814 (Chilopoda, Scolopendromorpha) from Movile Cave, Romania.

A new species of Cryptops Leach, 1814, C. speleorexsp. nov., is described from Movile Cave, Dobrogea, Romania. The cave is remarkable for its unique ecosystem entirely dependent on methane- and sulfur-oxidising bacteria. Until now, the cave was thought to be inhabited by the epigean species C. anomalans, which is widespread in Europe. Despite its resemblance to C. anomalans, the new species is well-defined morphologically and molecularly based on two mitochondrial (cytochrome c oxidase subunit I COI and 16S rDNA) and one nuclear (28S rDNA) markers. Cryptops speleorex sp. nov. shows a number of troglomorphic traits such as a generally large body and elongated appendages and spiracles, higher number of coxal pores and saw teeth on the tibia of the ultimate leg. With this record, the number of endemic species known from the Movile Cave reaches 35, which ranks it as one of the most species-rich caves in the world.

The Wynberg Cave System, the most important site for cave fauna in South Africa at risk

The Wynberg Cave System, located on the Cape Peninsula, represents one of the most significant sites of cave fauna in southern Africa. However, the continuous increase in cave visitation is severely impacting the system as evidenced by graffiti, the trampling and destruction of cave habitats and even a reduction in the sizes of bat colonies. In October 2019, the Wynberg Cave System was visited by a group of scientist, who discovered unregistered troglomorphic species. This, subsequently increased the number of troglobites occurring in the system to 19, which likely means that this system has the potential to become the first hotspot of subterranean biodiversity in Africa. Protecting the Wynberg Cave System is therefore of great importance. Here, we propose short and long-term strategies that include educating local communities on the importance of conserving caves and installing gated entrances.

A remarkable new troglobitic Parobisium (Pseudoscorpiones: Neobisiidae) from California

A new species of the pseudoscorpion genus Parobisium, P. petilum, is described from a cave in Shasta County, northern California. It is the most troglomorphic species of the genus with remarkably slender pedipalpal segments.

A new troglomorphic species of Trichomycterus (Siluriformes: Trichomycteridae) from north-eastern Colombia, with proposal of a new Trichomycterus subclade and remarks on some nominal species from Colombia.

Trichomycterus spectrum is described as a new species from the Alejo cave, drained by the Ranchería River basin, in La Guajira department, north-eastern Colombia, and is the first troglomorphic species described from this region. The new species shows an advanced degree of troglomorphisms expressed as eyes absent, long barbels and body depigmented. Trichomycterus spectrum is diagnosed by the putatively autapomorphic presence of a posterior process at the anterolateral corner of the epioccipital, and is also recognized by the derived presence of a circular foramen on the neural spine of the complex vertebra and the following posterior vertebra, and by the apomorphic presence of a well-developed coracoid bridge, distally expanded, and contacting or almost reaching the lateral margin of the cleithrum. The new species also shows the derived origin of the levator internus 4 on the dorsal surface of the posttemporo-supracleithrum that supports Trichomycterinae monophyly. We also propose a monophyletic subgroup provisionally within Trichomycterus, here named the Trichomycterus taenia species group, which includes species distributed in cis- and trans-Andean drainages in northern South America. The taxonomic status of several recently described nominal species from Colombia is discussed, with several synonymy proposals. RESUMEN: Trichomycterus spectrum es descrito como una especie nueva de la cueva de Alejo, drenada por la cuenca del río Ranchería, en el departamento de La Guajira, noreste de Colombia, y es la primera especie troglomórfica descrita para esta región. La especie nueva exhibe un grado avanzado de troglomorfismos expresado como ojos ausentes, barbillas largas y cuerpo depigmentado. Trichomycterus spectrum es diagnósticado por la presencia putativamente autapomórfica de un proceso posterior en la esquina anterolateral del epióticoy es reconocido también por la presencia derivada de un foramen circular en la espina neural de la vértebra compleja y de la vértebra posterior siguiente, y por la presencia apomórfica de un puente coracoideo bien desarrollado, expandido distalmente y contactando o muy próximo al margen lateral del cleitro. La especie nueva también posee el origen derivado del levator internus 4 sobre la superficie dorsal del posttemporo-supracleitro que soporta la monofilia de Trichomycterinae. También proponemos un subgrupo monofilético provisionalmente dentro de Trichomycterus, denominado aquí como el grupo de especies Trichomycterus taenia, el cual incluye especies distribuidas en cuencas cis y transandinas en el norte de Sudamérica. El estatus taxonómico de varias especies nominales recientemente descritas de Colombia es discutido, con varias propuestas de sinonimia.

Two new species and new records of terrestrial isopods (Crustacea, Isopoda, Oniscidea) from Brazilian caves

To date, approximately 190 species of terrestrial isopods are known from Brazil and only 14 are considered troglobiotic. After the examination of a large collection from caves in Bambuí and Una geomorphological areas, along the states of Bahia, Minas Gerais and Goiás, two new troglobiotic species were recognized. Pectenoniscus liliae Campos-Filho, Bichuette Taiti sp. n. (Styloniscidae) is described from Serra do Ramalho karst area, and Benthana xiquinhoi Campos-Filho, Bichuette Taiti sp. n. (Philosciidae) from sandstone caves of Chapada Diamantina region. The latter constitutes the second troglomorphic species of the genus. Xangoniscus aganju (Styloniscidae) is also recorded from two caves in the Serra do Ramalho karst area. The systematic position of Iuiuniscus iuiuensis is briefly discussed and Venezillo congener (Armadillidae) is redescribed from São Domingos karst area.

Coecobryasirindhornae sp. n., the most highly troglomorphic Collembola in Southeast Asia (Collembola, Entomobryidae).

The most highly troglomorphic Collembola of Southeast Asia, Coecobryasirindhornaesp. n., is described from a cave in Satun province, Thai Peninsula. It is characterised by its large size, extremely elongated antennae, relatively long legs and furca, reduced macrochaetotaxy, very long and slender claw, pointed tenent hair, four sublobal hairs on outer maxillary lobe, and the absence of eyes and pigmentation. A checklist of Thai Coecobrya species and a key to the troglomorphic species of Thailand are provided. Troglomorphy and conservation of cave habitats in the area are discussed.

The cave-dwelling dipluran (Diplura, Campodeidae) on the edge of the Last Glacial Maximum in Vancouver Island caves, North America (Canada)

A new cave-dwelling dipluran of the North American endemic genus Haplocampa is described, coming from a couple of caves excavated in a small limestone karstic area near Port Alberni, Vancouver Island (British Columbia, Canada). To Haplocampa belong five soil-dwelling species. L. M. Ferguson cited no less than eight more species living in soil and cave habitats in several US states but without producing any formal descriptions. Haplocampa, in spite of its large lateral crests on the unequal claws, has clear taxonomical features as a Campodeinae and is closely related with the cave-dwelling Pacificampa and Eumesocampa genera, due to sharing similar macrosetae body distribution and absence or reduction of the lateral process. The new proposed species, Haplocampawagnelli Sendra, sp. n., is rather interesting for its troglomorphic features: antennae with 32 antennomeres; olfactory chemoreceptors, each a multiperforated, folded-spiral structure; and numerous gouge sensilla. In addition, it is one of the northernmost troglomorphic species to have colonised – presumably recently – an area occupied by the Late Wisconsinian North America ice sheet during the Last Glacial Maximum. Furthermore, the close affinities between Haplocampa, Pacificampa (from caves in the extreme east of continental Asia and the southern Japanese Islands), Metriocampa (from the east of Asia and North America) and Eumesocampa (endemic to North America) suggest probable dispersal events over the Bering Land Bridge.

New species reveal unexpected interspecific microhabitat diversity in the genus Uthina Simon, 1893 (Araneae : Pholcidae)

Representatives of the Southeast Asian pholcid spider genus Uthina Simon, 1893 have been thought to be very homogeneous in their ecology and morphology. The 14 previously known species all inhabit near-ground microhabitats and cave entrances, and range from pale to dark brown in colour. Even their genitalia are partly very similar, with some species pairs being barely distinguishable based on morphological characters. Here we describe three new species from Bali, Java and Sulawesi that represent three further microhabitats and demonstrate considerable ecological and morphological diversity within the genus: U. maya, sp. nov. from Bali is a large dark species on tree trunks; U. hylobatea, sp. nov. from Bali and eastern Java is a pale leaf-dwelling species that exhibits colour dimorphism; and U. mimpi, sp. nov. is a pale troglomorphic species collected in the aphotic zones of two South Sulawesi caves. In addition, we present new data for five previously described species, including ultrastructure, natural history, new records, taxonomic notes and a description of the previously unknown female of Uthina khaosokensis Yao, Li & Jäger, 2014. Molecular data suggest that all previously described species are very closely related to each other (constituting the monophyletic luzonica-group), and that the three new species represent separate clades within the genus. However, the basal trichotomy could not be resolved: U. maya + (U. hylobatea + U. mimpi) + luzonica-group.

Phylogeny of the genus Pseudosinella (Hexapoda, Collembola) from the Western Carpathians caves reveals Miocene diversification

The observations from the recent period revealed that the Western Carpathians, a part of the Carpathian mountain chain, is the northernmost region in Europe with the occurrence of the obligate cave fauna. The collembolan genus Pseudosinella Schäffer, 1897 is a polyphyletic taxon derived from the genus Lepidocyrtus Bourlet, 1839 from which it differs in reduced number of eyes. It covers about 350 species with predominantly Holarctic distribution of which about 39% are confined to caves. We studied the morphology and molecular traits to identify cave species of the genus Pseudosinella occupying the Western Carpathian caves and clarify their phylogenetic relationships. Based on morphological traits we hypothesized that Pseudosinella aggtelekiensis (Stach, 1929) and P. paclti Rusek, 1961 are descendants of the different phyletic lineages, the former species lacking morphologically related edaphic species. On the other hand, several species related to P. paclti were found in caves, superficial subterranean habitats and in the soil. Molecular phylogeny analysis has shown two distinct groups of cave species following pattern of allopatric distribution. The first group consisted of populations of P. aggtelekienis from the Slovak Karst and an undescribed species from fragmented and isolated karst in eastern Slovakia. In the second group different populations of P. paclti occupying caves of the central karst regions were incorporated together with a new highly troglomorphic species confined to a small karst area. After an approximate estimate of the geological timing of the species isolation (RelTime), the two distinct Pseudosinella lineages separated approx. 9.54 mya followed by subsequent diversification in P. paclti lineage 8.36 mya, and in P. aggtelekiensis lineage 6.99 mya. This study contributed to assumption that the Western Carpathian Mts played an important role as speciation centre of the obligate cave fauna in Europe.

Annotated checklist of Gonyleptoidea (Opiliones: Laniatores) associated with Brazilian caves.

In Brazil, the order Opiliones has been well studied, making this country the leader in research with the group, but few extensive works have been made on the distribution of harvestmen associated with caves. In this context, the present paper aims to list all records of the superfamily Gonyleptoidea associated with Brazilian caves, using records from the literature and unreported data from scientific collections. The compiled checklist contains the largest number of harvestmen species recorded for caves in one country, worldwide. A total of 155 species belonging to 7 families were recorded from 952 caves throughout 152 municipalities and 17 states of Brazil. A considerable number of 46 putative (undescribed) new species were recognized, including 9 troglomorphic species. Additionally, 161 new municipal records where found for 58 known species. The most diverse family was Gonyleptidae (104 spp.), with the subfamilies Pachylinae (55 spp.), followed by Goniosomatinae (18 spp.) and Mitobatinae (16 spp.). The number of described species analysed in the present work represents about 12% of the Brazilian opiliofauna of Gonyleptoidea, with many species widely distributed, being indicative of affinity of the group with the cave environments. Thus, the compilation of distribution data of such species (mainly the troglobitic and troglomorphic) can directly contribute to a higher valuation of their habitats, leading to better preservation policies, as well as being useful for future ecological and biogeographical studies.

A new highly troglomorphic Loxosceles (Araneae: Sicariidae) from Brazil.

The spiders of the genus Loxosceles have been reported from caves in several regions of the world. Despite their commonness in subterranean habitats, the occurrence of troglomorphic species is quite rare. A new cave-dwelling species found in the Brazilian Caatinga can be included in the restricted list of troglomorphic Loxosceles by presenting the following troglomorphic traits: eyes with reduced diameter, absence of pigment around the eyes, appendage elongation and pale coloration. Thus, the aim of this study is to describe a new highly troglomorphic species of Loxosceles from Brazil, corresponding to the first troglomorphic species from South America. Loxosceles troglobia sp. nov. belongs to the gaucho group and can be distinguished from the other species of this group mainly by the presence of the troglomorphic characteristics mentioned above and by the shape of the female spermathecae and the male palp. The morphological traits, together with the fact that the new species was found only in inner and very humid portions of two nearby caves, indicate that it is troglobitic.