Global biodiversity and phylogenetic evaluation of remipedia (crustacea)

Remipedia is one of the most recently discovered classes of crustaceans, first described in 1981 from anchialine caves in the Bahamas Archipelago. The class is divided into the order Enantiopoda, represented by two fossil species, and Nectiopoda, which contains all known extant remipedes. Since their discovery, the number of nectiopodan species has increased to 24, half of which were described during the last decade. Nectiopoda exhibit a disjunct global distribution pattern, with the highest abundance and diversity in the Caribbean region, and isolated species in the Canary Islands and in Western Australia. Our review of Remipedia provides an overview of their ecological characteristics, including a detailed list of all anchialine marine caves, from which species have been recorded. We discuss alternative hypotheses of the phylogenetic position of Remipedia within Arthropoda, and present first results of an ongoing molecular-phylogenetic analysis that do not support the monophyly of several nectiopodan taxa. We believe that a taxonomic revision of Remipedia is absolutely essential, and that a comprehensive revision should include a reappraisal of the fossil record.     

A new cave-dwelling and endemic species of the genus Pholeuonopsis (Coleoptera, Leiodidae) from Serbia

In the present study, a new species of a cavernicolous beetle is described from Serbia: Pholeuonopsis (Pholeuonopsis) zlatiborensis sp. n. (Leptodirini, Cholevinae, Leiodidae). All important taxonomic features have been thoroughly analyzed and illustrated. The new species probably belongs to an old phyletic lineage of mesogeid origin, like other known Pholeuonopsis species inhabiting cave and endogean habitats in the western part of the Balkan Peninsula. Therefore, the species is both relict and endemic inhabitant of cave habitats in Serbia.     

Diurnal dynamics of the microbial loop in peatlands: structure, function and relationship to environmental parameters

Globally, introductions of alien species are increasingly common, with invasive predators potentially having detrimental effects via predation on native species. However, native prey may avoid predation by adopting new behaviors. To determine whether invasive fish populations consume endemic shrimp in invaded Hawaiian anchialine habitats or if adopted patterns of diel migration prevents predation as previously hypothesized, a total of 183 invasive poeciliids (158 Gambusia affinis and 25 Poecilia reticulata) were collected for gut content analyses from four anchialine sites during wet and dry seasons on the islands of Hawai‘i and Maui. Predation on shrimp was not detected in habitats where they retreat exclusively into the underlying aquifer diurnally and only emerge nocturnally. However, low levels of predation were detected (7/65 fishes, only by Gambusia affinis) at Waianapanapa Cave, Maui, where shrimp retreat into both the aquifer and a cave during the day. Thus, adopted behavioral responses to invasive fishes generally, though not universally, prevent predation on endemic Hawaiian anchialine shrimps. However, non-consumptive effects resulting from behavioral modification of shrimps may have appreciable impacts on the Hawaiian anchialine ecosystem and warrant further study.     

Micropacteridae, a new family of Remipedia (Crustacea) from the Turks and Caicos Islands

Recent diving explorations of anchialine caves on the Turks and Caicos Islands yielded a rather small and slender new species of Remipedia. Micropacter yagerae n. gen., n. sp. is distinguished from all other species of nectiopod remipedes by a number of autapomorphic characters, including an oval body terminus with fused segments, unequal pairs of terminal claws on maxilla and maxilliped, an almost complete reduction of sternal bars and pleurotergites, molar processes with relatively few, but strong spines, and frontal filaments with bifurcate processes. Based on the unique combination of derived and primitive characters, we propose to erect a new family, Micropacteridae, for this new species and genus of Remipedia. Taxonomic diagnoses for the class Remipedia, order Nectiopoda (emended due to discovery that the maxilliped is 9-segmented), and for the families Speleonectidae and Godzilliidae are presented and discussed.     

Speleohvarella gamulini gen. et sp. nov., a new copepod (Calanoida, Stephidae) from an anchialine cave in the Adriatic Sea

A new copepod genus and species, Speleohvarella gamulini, collectedfrom the anchialine cave iva Voda on Hvar Island (Croatia),is described from both sexes. This is the first record of acalanoid copepod found in an Adriatic anchialine cave. The newgenus is distinguished from other Stephidae by a combinationof the following features: the cephalosome is separate fromthe first pedigerous somite, and the fourth and fifth pedigeroussomites are fused; the female urosome has 4 segments, the genitaldouble-somite is symmetrical and the caudal rami is asymmetricalwith the right longer than the left; antennules of both sexesare symmetrical and 24-segmented, with the fusion of ancestralsegments II–IV, X–XI and XXVII–XXVIII; theexopod of antenna is 7-segmented; 2 setae are present on thebasal exite of maxillule; in the male the right leg 5 is shortand 3-segmented, and the left leg elongate and 5-segmented.     

Genetic exchange between anchialine cave populations by means of larval dispersal: the case of a new gastropod species Neritilia cavernicola

Despite being limited to caves, many anchialine taxa have disjunct insular distributions, which raises questions about their origins and colonization history. This study deals with the new gastropod Neritilia cavernicola sp. n. (Neritopsina: Neritiliidae) from anchialine caves on two islands in the Philippines that are separated by the deep Bohol Strait and situated 200 km apart along the coastline of Cebu Island. Neritilia cavernicola is an obligate stygobiont and most closely resembles Neritilia littoralis , which lives in interstitial waters of the Nansei-shoto Islands, Japan. Its eggs and larval shells are identical to those of other Neritilia species, despite their different adult habitats. This suggests a marine planktotrophic phase (as occurs in amphidromous riverine species of Neritilia ), and consequent migration between islands via ocean currents. Here we present the first genetic structure for anchialine cave organisms; comparisons of 1276 bp sequences from mitochondrial cytochrome oxidase I show no evidence of genetic isolation between the islands. All individuals evidently are part of a panmictic population and the low vagility of adults and their seemingly isolated cave habitats do not limit gene flow in N. cavernicola . This migration model, based on marine larval dispersal, may be widely applicable to anchialine stygobites with insular distributions, as many such organisms (including shrimps, crabs and fishes) are phylogenetically allied to amphidromous species.     

An Unique Anchialine Pool in the Hawaiian Islands

The Sailor's Hat crater was artificially formed on the south coast of Kaho'olawe Island in 1965 with explosives. The explosion formed a crater about 50 m from the shoreline, which penetrates the watertable to a 5 m depth. The pool at the bottom of the crater meets the criteria of an anchialine pond because it shows tidal fluctuation, has measurable salinity, and lacks surface connections to the sea. The water chemistry of this pool is similar to the ocean except silica is elevated and salinity is slightly depressed suggesting a small groundwater influence. The fauna is dominated by waterboatmen, an endemic shrimp and tubeworm, polychaetes, amphipods, an ostracod, gastropod, solitary ectoproct. anemone, flatworm and sponge. The atyid shrimp, Halocaridina rubra, is a characteristic species of Hawaiian anchialine systems and probably colonized this 32-year old pool by active migration via the watertable. Colonization by the remaining fauna may have occurred by storm surf (for marine species) or with the wind. Most predators are unable to inhabit anchialine ponds because of difficult access due to physical barriers, or to unsuitable ecological conditions. The anchialine habitat and life history strategy of the atyid shrimp have probably been important influences on the adaptative success of H. rubra in the Hawaiian Islands, and may be important characteristics of hypogeal anchialine species elsewhere.     

Rocks and clocks: linking geologic history and rates of genetic differentiation in anchialine organisms

The geologic history of a region can significantly impact the development of its flora and fauna, with past events shaping community patterns and evolutionary trajectories of species. In this context, islands are excellent “natural laboratories” for studying the fundamental processes of evolution due to their discrete geographical nature and dynamic geologic histories. An island system meeting these criteria is the Hawaiian Archipelago, which is ideal for testing how island geologic history influences the processes leading to population genetic variation and differentiation. One Hawaiian endemic whose evolutionary history is closely tied to the geology of the islands is the anchialine atyid shrimp Halocaridina, whose mitochondrial cytochrome oxidase I (COI) gene is hypothesized to be evolving at the rate of 20% per million years. To validate this rapid evolutionary rate, time since divergence estimates between geographically close, yet genetically distinct, populations were calculated for Halocaridina from anchialine habitats on the islands of Hawai’i, Maui, and O’ahu. On the younger (i.e., <1.5 million years) islands of Hawai’i and Maui, where all anchialine habitats occur in basalt, application of the Halocaridina molecular clock identified a strong correlation between levels of genetic divergence and the geologic age of the region inhabited by those populations. In contrast, this relationship weakened when similar analyses were conducted for Halocaridina from limestone anchialine habitats on the older (i.e., >2.75 million years) island of O’ahu. These results suggest geologic age, basin origin and/or composition are important factors that should be taken into consideration when conducting molecular clock analyses on anchialine flora and fauna as well as island populations in general.     

Shrimps down under: evolutionary relationships of subterranean crustaceans from Western Australia (Decapoda: Atyidae: Stygiocaris)

Background

We investigated the large and small scale evolutionary relationships of the endemic Western Australian subterranean shrimp genus Stygiocaris (Atyidae) using nuclear and mitochondrial genes. Stygiocaris is part of the unique cave biota of the coastal, anchialine, limestones of the Cape Range and Barrow Island, most of whose nearest evolutionary relations are found in coastal caves of the distant North Atlantic. The dominance of atyids in tropical waters and their food resources suggest they are pivotal in understanding these groundwater ecosystems.

Methodology/Principle Findings

Our nuclear and mitochondrial analyses all recovered the Mexican cave genus Typhlatya as the sister taxon of Stygiocaris, rather than any of the numerous surface and cave atyids from Australia or the Indo-Pacific region. The two described Stygiocaris species were recovered as monophyletic, and a third, cryptic, species was discovered at a single site, which has very different physiochemical properties from the sites hosting the two described species.

Conclusions/Significance

Our findings suggest that Stygiocaris and Typhlatya may descend from a common ancestor that lived in the coastal marine habitat of the ancient Tethys Sea, and were subsequently separated by plate tectonic movements. This vicariant process is commonly thought to explain the many disjunct anchialine faunas, but has rarely been demonstrated using phylogenetic techniques. The Cape Range''s geological dynamism, which is probably responsible for the speciation of the various Stygiocaris species, has also led to geographic population structure within species. In particular, Stygiocaris lancifera is split into northern and southern groups, which correspond to population splits within other sympatric subterranean taxa.     

Copepods from ground waters of Western Australia, VII. Nitokra humphreysi sp. nov. (Crustacea: Copepoda: Harpacticoida)

Nitokra humphreysi sp. nov. (Harpacticoida: Ameiridae) is described from anchialine ground waters of the Cape Range karst area in northwestern Australia. The new species belongs to those species of the genus Nitokra Boeck, 1865 with a reduced number of spines/setae on the basoendopodite of the female fifth leg. It is remarkably similar to N. reunionensis Bozic, 1969 and to N. laingensis Fiers, 1986, but there are clear distinguishing features. Nitokra humphreysi sp. nov. has clear stygomorphic features, being colourless and lacking the nauplius eye.     

Multiple cave invasions by species of the planthopper genus Oliarus in Hawaii (Homoptera: Fulgoroidea: Cixiidae)

Although geologically young, the Hawaiian Islands harbour a rich and remarkably diverse fauna of terrestrial troglobites: more than 70 cave species are known from Kauai, Oahu, Molokai, East Maui, and Hawaii Island. Among the more speciosc groups that have invaded the subterranean biome are the planthoppers (Homoptera Cixiidae) of the genus Oliarus. Five new obligately cavernicolous (troglobitic) Oliarus species which differ in their degree of troglomorphy and male genital structures, are described from lava tubes on the Hawaiian Islands: O. lorettae sp. nov. and O. makaiki sp. nov. from Hawaii Island, O. gagnei sp. nov. and O. ivaikau sp. nov. from Maui Island, and O. kalaupapae sp. nov. from Molokai Island. Short diagnoses of the two troglobitic species already known, 0. polyphemus Fennah, 1973 from Hawaii Island and 0. priola Fennah, 1973 from Maui are provided. Notes on the ecology and distribution of all cavernicolous species are given. Morphological evidence suggests that each of the seven cavernicolous Oliams species from Hawaii represents a separate, independent adaptive shift to underground environments. Potential relationships to the extant epigean species are discussed.     

Patterns of genetic connectivity among anchialine habitats: a case study of the endemic Hawaiian shrimp Halocaridina rubra on the island of Hawaii

Anchialine habitats, landlocked bodies of mixohaline water that fluctuate with the tides but have no surface connection to the sea, are known from around the world. Many anchialine organisms have widespread distributions and it has been hypothesized that high levels of gene flow and low levels of genetic differentiation are characteristic of populations from these habitats. However, the generality of this hypothesis requires further assessment, particularly in light of the significant negative impact these habitats and their biota have experienced from anthropogenic causes. This study investigated the population structure and demography of an endemic Hawaiian anchialine species, the atyid shrimp Halocaridina rubra, using mitochondrial cytochrome c oxidase subunit I (COI) gene sequences. A survey of 305 individuals from 16 populations collected on the island of Hawaii revealed 135 haplotypes. These haplotypes belonged to one of two divergent (2.7-4.9%) lineages; notably, no haplotypes were shared between the two coasts of the island. Along each coast, strong subdivision and little to no gene flow occurs between populations separated by > 30 km. The population structure and demography of H. rubra on Hawaii are influenced by regional hydrology, geology, volcanism and two distinct colonization events of the island. Thus, H. rubra on Hawaii demonstrates that populations of endemic anchialine organisms may exhibit significant levels of genetic structure and restricted levels of gene flow over limited geographic scales. This report brings novel insight into the biology of anchialine organisms and has important implications for the future management of these habitats and their biota.     

Comparative Density of Hair Sensilla on the Legs of Cavernicolous and Epigean Harvestmen (Arachnida: Opiliones)

To allow an animal to behave appropriately, the location of sensorial structures is expected to be related to their function. As the different leg pairs of arachnids may have different functions (probing x supporting the body), one could expect them to have a different density of sensilla. Moreover, different regions of the same leg (dorsal, lateral, and ventral) would also be expected to have different densities of sensilla, according to the use of each region (e.g., the ventral part is often in contact with the substrate while the dorsal part is not). As cavernicolous animals are expected to be more sensitive than their epigean relatives, one could also expect a different density of sensilla when comparing cavernicolous and epigean animals. Using three epigean and three cavernicolous species of harvestmen (Arachnida, Opiliones), this study aimed at describing the morphology of hair sensilla on the legs and answering three questions: (1) Are there differences in the density of hair sensilla between the dorsal, lateral and ventral regions of each leg pair of the same individual? (2) Are there differences in the density of hair sensilla between the leg pairs of the same individual? (3) Are there differences in the density of hair sensilla when comparing the leg pairs of individuals of cavernicolous and non-cavernicolous species? The tarsi and metatarsi of all right legs of the six studied species were analyzed under a scanning electron microscope. The results (P < 0.05) showed that, in general: the ventral region of the tarsus was denser in sensilla trichodea than the lateral and dorsal regions, particularly on legs I and II; the density of sensilla chaetica did not differ on legs III and IV, but was greater on the dorsal region of legs I and II; the ventral part of legs I had the higher density of sensilla trichodea of the four pairs, whereas the second pair had the lower density; Holcobunus citrinus (Eupnoi) was the species with higher density of sensilla trichodea, on all legs; the cavernicolous species had a lower density of sensilla than the epigean species. The results are tentatively related to harvestmen behavior.     

Description of a new species of bat-associated argasid tick (Acari: Argasidae) from Brazil

A new species of argasid tick (Acari: Argasidae) is described from immature and adult specimens collected from several localities in Brazil. A complete morphological account is provided for all postembryonic life stages, i.e., larva, nymph, female, and male. Ornithodoros cavernicolous n. sp. is the 113(th) in the genus. Morphologically, the new species shares common features, e.g., presence of well-developed cheeks and legs with micromammillate cuticle, with other bat-associated argasid ticks included in the subgenus Alectorobius. In particular, the new species is morphologically related to Ornithodoros azteci Matheson, with which it forms a species group. Phylogenetic analysis based on the 16S rRNA gene sequences supports the placement of the new species within a large clade that includes other New World bat-associated argasids. However, the new species seems to represent an independent lineage within the genus Ornithodoros.     

Void development on carbonate coasts: creation of anchialine habitats

Anchialine caves in coastal locations develop in two ways: by pseudokarst processes that form talus caves, sea caves, tafoni, fissure caves and lava tubes, and by karst dissolutional processes that form stream caves, flank margin caves, and blue holes. Pseudokarst caves are of minor importance in anchialine cave habitat development, with some lava tubes being notable exceptions. Dissolution caves provide the most extensive, variable, and long-term environments for anchialine habitats. The Carbonate Island Karst Model (CIKM) allows dissolutional cave development in carbonate coasts to be understood as the interplay between freshwater and marine water mixing, sea-level change, rock maturity, and interaction with adjacent non-carbonate rocks. Glacioeustatic sea-level changes of the Quaternary have moved all coastal anchialine cave environments repeatedly through a vertical range of over 100 m, and modern anchialine environments could not develop at their current elevations until ~4,000 years ago when sea level reached its present position. Blue holes form by a variety of mechanisms, but the most common is upward stoping and collapse from deep dissolutional voids. As a result, they provide vertical connection between different levels of horizontal cave development produced by a variety of earlier sea-level positions. Blue holes are overprinted by successive sea-level fluctuations; each sea-level event adds complexity to the habitats within blue holes and the cave systems they connect. Blue holes can reach depths below the deepest glacioeustatic sea-level lowstand, and thereby provide a refugia for anchialine species when cave passages above are drained by Quaternary sea-level fall. Blue holes represent the most significant anchialine cave environment in the world, and may provide clues to anchialine cave species colonization and speciation events.     

Colopha hispanica sp.n. (Homoptera: Aphidoidea: Pemphigidae): an unusual endophytic aphid living inside the stems of Scirpus holoschoenus (Cyperaceae)

Abstract. A new aphid species of the genus Colopha (Pemphigidae: Eriosomatinae), Colopha hispanica is described from Spain. The apterae differ from those of other species of Colopha in the shortness of their antennae and legs, in the greater number of their wax glands and in the underdevelopment of the setal socket on the forelegs. These aphids live inside the stems of Scirpus holoschoenus (Cyperaceae); this is the first record of a truly endophytic aphid. The adults are immobile. C. hispanica is compared with the other known species of Colopha , with Kaltenbachiella pallida , a similar species also found in Spain and with Gharesia polunini , a primitive species of Eriosomatinae. The distribution and host plants of Colopha species are reviewed and discussed.     

Marine Lake Mogilnoe (Kildin Island,the Barents Sea): one hundred years of solitude

Lake Mogilnoe (Kildin Island, the Barents Sea) is a marine stratified lake, a refuge for landlocked populations of marine organisms. Unlike other known marine lakes from polar areas, which communicate with the sea by water percolation at the surface, Mogilnoe has a subterranean connection with the sea like tropical and subtropical anchialine lakes. Similarly to some other marine lakes, Mogilnoe has traditionally been considered to be biologically isolated from the sea and subject to little change. We review the current status of the physical features, zooplankton and benthos of Mogilnoe and trace changes that have occurred in the lake since the start of observations in 1894. The anaerobic bottom water layer has expanded by 100 %, while the upper freshwater layer has diminished by 40 %. The species diversity of zooplankton and macrobenthos has halved. The occurrence of Atlantic cod likens Mogilnoe to some other Arctic marine lakes while the presence of large flocks of sea anemones, scyphomedusae and suberitid sponges makes it similar to tropical anchialine lakes. Lake Mogilnoe is not entirely biologically isolated; accidental introduction of species from the sea does occur. We argue that the idealised model of an isolated steady-state ecosystem can be applied to a marine lake with caution. A model of fluctuating abiotic environment and partial biological isolation portrays the real situation better.     

Troglobitic scorpions: a new genus and species from Brazil

A new genus and species of troglobitic buthid scorpion are described on the basis of a single specimen collected in Brazil. This is the first cavernicolous scorpion ever found in Brazil, and only the second to be found in South America. Some considerations on troglobitic scorpions are proposed.     

Phylogeography of cave pseudoscorpions in southern Australia

Aim  To investigate molecular phylogenetic divergence and historical biogeography of the cave-dwelling pseudoscorpion genus Protochelifer.
Location  Caves and nearby epigean habitats in southern Australia were sampled from western Victoria, Naracoorte Caves, Flinders Ranges, Kangaroo Island, Nullarbor Plain and south-west Western Australia.
Methods  Allozyme electrophoresis (57 individuals) and a 569-base-pair section of the mtDNA COI gene (22 individuals) were used to reconstruct phylogenetic relationships among four cave species and three epigean species from 13 locations.
Results  Phylogenetic reconstruction using the allozyme and mtDNA sequence data revealed a similar topology, showing recent speciation of several Protochelifer populations in caves from Naracoorte to the Nullarbor Plain. Naracoorte Caves contained a single species, Protochelifer naracoortensis , found in four separate caves, while all other cave species appear to be restricted to single caves.
Main conclusions  At a local scale, as indicated by the four Naracoorte caves, dispersal is thought to occur via micro- and mesocaverns, and possibly by phoresy using insect or bat vectors. With current data we are unable to determine if cavernicolous species of Protochelifer have arisen from a single cave colonization event followed by phoretic dispersal on bats to other caves, or multiple cave-invasion events from independent epigean ancestors. Genetic heterogeneity among Protochelifer populations from Nullarbor caves suggest that P. cavernarum , the only species presently recorded from this region, is likely to constitute a species complex requiring further study to fully resolve its relationships.     

A new species of Thetispelecaris (Crustacea: Peracarida) from submarine cave on Grand Cayman Island

A new species of the peracaridan order Bochusacea, Thetispelecaris yurikago, is described from a submarine cave on Grand Cayman Island, the Caribbean Sea. The new species is the fourth species of the order and family, and the second of the genus. Recent studies have strongly suggested a close phylogenetic affinity between cave-dwelling and deep-sea taxa in the Bochusacea as recognized in other cavernicolous/deep-sea crustaceans such as amphipods and copepods. The morphology of the gut and female reproductive system is observed for the first time in the Bochusacea: the stomach is complex with structures such as ridges, processes, spinules, and hairs in the lumen; paired gonopores are located near the base of the fifth pereiopods on the sternite.