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.     

Phylogenetic analysis of Remipedia (Crustacea)

We present a cladistic analysis of the crustacean class Remipedia, including all 17 extant species currently assigned to the order Nectiopoda, with the Carboniferous fossil Tesnusocaris serving as an outgroup. We applied different methodological approaches and coding options to a basic matrix composed of 26 morphological characters. Our analyses strongly support monophyly of the Godzilliidae and affirm justification of the family Micropacteridae. However, the present taxonomic structure within the Speleonectidae is partly incompatible with our results, and we cannot exclude that the family is paraphyletic.     

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.     

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.     

Post-embryonic development of remipede crustaceans

During diving explorations of anchialine cave systems on Abaco Island, Bahamas, we collected five larvae that represent different developmental stages of remipede crustaceans. Based on four early naupliar stages and a post-naupliar larva, it is possible for the first time to reconstruct the postembryonic development of Remipedia some 25 years after their discovery. These specimens begin to fill in some critical gaps in our knowledge of this important group of crustaceans.     

The biogeochemistry of anchialine caves: progress and possibilities

Recent investigations of anchialine caves and sinkholes have identified complex food webs dependent on detrital and, in some cases, chemosynthetically produced organic matter. Chemosynthetic microbes in anchialine systems obtain energy from reduced compounds produced during organic matter degradation (e.g., sulfide, ammonium, and methane), similar to what occurs in deep ocean cold seeps and mud volcanoes, but distinct from dominant processes operating at hydrothermal vents and sulfurous mineral caves where the primary energy source is mantle derived. This review includes case studies from both anchialine and non-anchialine habitats, where evidence for in situ chemosynthetic production of organic matter and its subsequent transfer to higher trophic level metazoans is documented. The energy sources and pathways identified are synthesized to develop conceptual models for elemental cycles and energy cascades that occur within oligotrophic and eutrophic anchialine caves. Strategies and techniques for testing the hypothesis of chemosynthesis as an active process in anchialine caves are also suggested.     

Pancrustacean phylogeny in the light of new phylogenomic data: support for Remipedia as the possible sister group of Hexapoda

Remipedes are a small and enigmatic group of crustaceans, first described only 30 years ago. Analyses of both morphological and molecular data have recently suggested a close relationship between Remipedia and Hexapoda. If true, the remipedes occupy an important position in pancrustacean evolution and may be pivotal for understanding the evolutionary history of crustaceans and hexapods. However, it is important to test this hypothesis using new data and new types of analytical approaches. Here, we assembled a phylogenomic data set of 131 taxa, incorporating newly generated 454 expressed sequence tag (EST) data from six species of crustaceans, representing five lineages (Remipedia, Laevicaudata, Spinicaudata, Ostracoda, and Malacostraca). This data set includes all crustacean species for which EST data are available (46 species), and our largest alignment encompasses 866,479 amino acid positions and 1,886 genes. A series of phylogenomic analyses was performed to evaluate pancrustacean relationships. We significantly improved the quality of our data for predicting putative orthologous genes and for generating data subsets by matrix reduction procedures, thereby improving the signal to noise ratio in the data. Eight different data sets were constructed, representing various combinations of orthologous genes, data subsets, and taxa. Our results demonstrate that the different ways to compile an initial data set of core orthologs and the selection of data subsets by matrix reduction can have marked effects on the reconstructed phylogenetic trees. Nonetheless, all eight data sets strongly support Pancrustacea with Remipedia as the sister group to Hexapoda. This is the first time that a sister group relationship of Remipedia and Hexapoda has been inferred using a comprehensive phylogenomic data set that is based on EST data. We also show that selecting data subsets with increased overall signal can help to identify and prevent artifacts in phylogenetic analyses.     

Anchialine Gyprididae (Ostracoda) from the Galapagos Islands, with a review of the subfamily Paracypridinae

The five species of Cyprididae collected from anchialine habitats of the Galapagos Islands include Paracypris crispa, previously described from marine caves and reefs on Bermuda, and the freshwater species Strandesia stocki, which is widely distributed in wells of the West Indies. Three new species, Dolerocypria ensigera, Mungava recta and Hansacypris galapagosensis, contribute to more precise understanding of these circumtropical genera. A review of known soft-anatomical characters for 68 species of Paracypridinae, five of which are transferred to different genera, reveals too many inconsistencies for a simple hypothesis. The current classification of Paracypridinae into three tribes and 18 genera may be overly subdivided, and elevation of Paracypridinae to family rank is not warranted.     

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.     

The dispersal and colonisation behaviour of the marine polychaete <Emphasis Type="Italic">Nereis diversicolor</Emphasis> (O. F. Müller) in south-east England

Recent submarine caves are inhabited by endemic faunas adapted to oligotrophism, darkness and a tranquil environment. Many of their representatives are archaic types of animals resembling fossils from very early times in evolution. This article compares fossil fauna from Jurassic neptunian dykes (originally sea bed clefts) from the Western Carpathians with the Recent cave-dwelling fauna. The ostracods Pokornyopsis feifeli are particularly important. In the Western Carpathians, these were exclusively found in the Middle/Late Jurassic fissure fillings, but in the non-Tethyan Germanic Jurassic this species was found in deep-marine claystones. They are phylogenetic forerunners of the recent genus Danielopolina inhabiting both anchialine caves and deep seas. This indicates a Jurassic migration of deep-marine fauna to cryptic habitats. Other examples of cryptic communities include the Upper Jurassic cavity-dwelling fauna dominated by serpulids and scleractinian corals. Associated suspension feeders include thecideidine brachiopods, oysters, bryozoans, sponges, crinoids and sessile foraminifers. Serpulid-dominated bioconstructions have recent analogies in the Mediterranean and Carribean seas. Different type of dyke communities represent the Late Jurassic fauna of small sized ammonites which originated from both Tethyan and Boreal paleobioprovinces. It has not been established whether these amonites were juvenile, dwarfed specimens adapted to limited cave space or size-sorted adult specimens.     

How might sea level change affect arthropod biodiversity in anchialine caves: a comparison of Remipedia and Atyidae taxa (Arthropoda: Altocrustacea)

Sea level change influences biodiversity of endemic cave fauna to varying degrees. In anchialine systems, a marine layer flows under less saline layers, each with differing associated fauna. We assess the role of present and historic (last glacial maximum – 18,000 years ago) distance from the ocean in determining species richness and phylogenetic diversity patterns for two groups of anchialine crustaceans: the marine-restricted Remipedia and a subset of groundwater-inhabiting atyid shrimp with greater tolerance for salinity variation. We calculated species richness and phylogenetic diversity per cave based on records of remipede and atyid diversity at 137 locations in the Yucatán Peninsula, Caribbean, Australia, and the Canary Islands. After calculating the distance of each cave’s surface opening from the past and present shoreline, we evaluated how species richness and phylogenetic diversity change with distance from the present and historic ocean. Remipede species richness and phylogenetic diversity declined rapidly with distance from the ocean. Ninety-five percent of the remipedes surveyed were located within 7 km of the present ocean and 18 km of the historic ocean. Atyid species richness and phylogenetic diversity declined more slowly with distance from the ocean than that of remipedes. Atyid shrimp were also distributed over a broader range: 95 % were located within 100 km of the present ocean and 240 km of the historic ocean. Our findings indicate that coastal geomorphology and salinity tolerance influence a clade’s distribution with respect to its distance from the ocean. We also report a possible latent response to sea level change.     

Danielopolina kornickeri sp. n. (Ostracoda, Thaumatocypridoidea) from a western Australian anchialine cave: morphology and evolution

Danielopolina kornickeri sp. n . is described from an anchialine cave in Western Australia. This is the first Danielopolina species occurring outside of the Western Hemisphere (Atlantic and Eastern Pacific Oceans and Islands). A cladistic analysis indicates that this species is a primitive taxon of the anchialine cavernicolous clade; the deep-sea dwelling species Danielopolina carolynae appears more primitive and does not cluster with the other Danielopolina species. The ecological environment of D. kornickeri is described. Detailed discussions consider: (1) the shell ornamentation and its relevance to the phylogeny of the Thaumatocyprididae; (2) the antero-dorsal node of the Permian Thaumatomma (hypothesized here to be an ocular lens which regressed in the post-Palaeozoic thaumatocypridids); (3) the distal chaetotaxy of the antennae (hypothesized to perform the chemosensorial function known in the aesthetascs of other myodocopids or podocopids); (4) palaeobiogeographical arguments for a shallow marine origin of cavernicolous species Danielopolina .     

Phytoplankton of cenotes and anchialine caves along a distance gradient from the northeastern coast of Quintana Roo,Yucatan Peninsula

This work details the taxonomic composition of suspended algae (phytoplankton and tycoplankton) communities in five cenotes (sinkholes) and two anchialine caves in northeastern Quintana Roo, Mexico. The sample set of cenotes are Casa, Nohoch Nah Chich, Maya Blue, Cristal, and Carwash, as well as the two associated caves leading from the cenotes of Maya Blue and Cristal. The site distribution represents a distance gradient with respect to the coastline with which we observe the effects of tidal movement and the mixing of waters (e.g. saline water and freshwater) on the composition of the suspended algae communities. Two sample sets were taken, one at the end of the dry season (March–April 1995) and the second at the end of the rainy season (September–October 1995) with the goal of comparing the contrasting climatic conditions of the region. A total of 79 species were identified, of which, diatoms were the most important with respect to species richness with a total of 75% of species. The floristic composition is very similar between the freshwater cenotes. The distance of a cenote site with respect to the coastline was a determining factor in the species composition. Casa Cenote is the most distinct of the sample set for the presence of marine species due to its proximity to the coastline. The tides are a large determining factor of the floristic composition of Casa Cenote with 24% all species identified in this study found exclusively in this system. The anchialine system species are transported from the cenotes and the adjacent cave systems. The largest percentage or species (95%) are freshwater, and only 5% of the total number of identified species are of marine origin. It is recognized that the most distant cenotes from the coast, Carwash and Cristal, as well as Maya Blue and Nohoch Nah Chich, are the most similar, despite being part of different cave systems. In these inland systems the marine species decreased drastically (2.4% in Nohoch Nah Chich and no marine species in the remaining cenotes). Marine species are found at the halocline of the caves.     

The post-embryonic development of Remipedia (Crustacea)—additional results and new insights

The post-embryonic development of a species of the enigmatic crustacean group Remipedia is described in detail for the first time under various aspects. Applying a molecular approach, we can clearly prove the species identity of the larvae as belonging to Pleomothra apletocheles. We document the cellular level of several larval stages and the differentiation of segments, limbs, and the general body morphology applying the techniques of confocal laser scanning microscopy and scanning electron microscopy. In addition, we document the swimming behavior and the peculiar movements of the naupliar appendages. A comparison of our results with published data on other Crustacea and their larval development tentatively supports ideas about phylogenetic affinities of the Remipedia to the Malacostraca. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users. An erratum to this article can be found at     

Evolution of cave suspension feeding in Protodrilidae (Annelida)

Protodrilidae belongs in a lineage that until now entirely consisted of deposit‐feeding, highly adapted interstitial annelids. Except for a pair of anterior palps, all protodrilids lack appendages, parapodia and chaetae; and have slender bodies adapted to glide between the sand grains by ciliary motion. The first exception to these characteristics is Megadrilus pelagicus n. sp. inhabiting the water column of the anchialine La Corona cave system in Lanzarote. Its morphology and evolutionary history are here investigated by combining observations from in vivo video recordings and advanced microscopy with phylogenetic analyses. Our studies revealed a unique pelagic, suspension feeding behaviour attained by its long ciliated palps in combination with an autopomorphic dorsal ciliated keel and several longitudinal and transverse ciliary bands. Phylogenetic analyses recovered Megadrilus pelagicus n. sp. nested within Protodrilidae indicating that its unique traits are derived within the family. These traits are traced in the tree topologies in correlation to cave colonization. The evolution of these traits can be functionally explained by the different demands of a pelagic suspension feeding strategy compared to the ancestral deposit‐feeding guild of the family. The origin of this suspension feeding strategy was presumably favoured by the partial isolation of the anchialine ecosystem, connected to the sea only through the highly porous volcanic subterranean bedrock. This crevicular connection limits the amount of predators and turbulence in the cave, but allows continuous water flow into the system carrying organic particles, which is the main source of food when photosynthetic primary production does not occur and sedimentation is limited. These conditions may select for pelagic suspension feeding as the most feasible life‐strategy in anchialine caves, which the dominance of pelagic, suspension feeding crustaceans and annelids in anchialine cave assemblages may also reflect. For species of ancestrally deposit‐feeding lineages entering the cave system, such as the annelid families Protodrilidae and Nerillidae, an adaptive‐shift from interstitial to crevicular habitats seemingly correlates with dramatic morphological changes and speciation. The dramatic changes observed in these primarily interstitial lineages compared to their relatives, point to alternative adaptive evolutionary pathways related to ecological fitness contrary to the previously proposed theories focusing on geological or stochastic processes.     

When phylogeny meets geology and chemistry: doubts on the dating of Ethiopian amber

The first fossil species of a Melissotarsus ant is described (Melissotarsus ethiopiensis n. sp.), suggesting that Ethiopian amber could be cenozoic rather than cretaceous. This hypothesis is supported by a Fourier transform infrared spectroscopy (FTIR) analysis of the amber itself, suggesting a weak maturation of the fossil resin, and a revision of the pyrolysis–gas chromatography–mass spectrometry (PY-GC-MS) analysis done by Schmidt and his collaborators in 2010, in an article in which the deposit was described for the first time.     

Mitochondrial OXPHOS genes provides insights into genetics basis of hypoxia adaptation in anchialine cave shrimps

Cave shrimps from the genera Typhlatya, Stygiocaris and Typhlopatsa (TST complex) comprises twenty cave-adapted taxa, which mainly occur in the anchialine environment. Anchialine habitats may undergo drastic environmental fluctuations, including spatial and temporal changes in salinity, temperature, and dissolved oxygen content. Previous studies of crustaceans from anchialine caves suggest that they have possessed morphological, behavioral, and physiological adaptations to cope with the extreme conditions, similar to other cave-dwelling crustaceans. However, the genetic basis has not been thoroughly explored in crustaceans from anchialine habitats, which can experience hypoxic regimes. To test whether the TST shrimp-complex hypoxia adaptations matched adaptive evolution of mitochondrial OXPHOS genes. The 13 OXPHOS genes from mitochondrial genomes of 98 shrimps and 1 outgroup were examined. For each of these genes was investigated and compared to orthologous sequences using both gene (i.e. branch-site and Datamonkey) and protein (i.e. TreeSAAP) level approaches. Positive selection was detected in 11 of the 13 candidate genes, and the radical amino acid changes sites scattered throughout the entire TST complex phylogeny. Additionally, a series of parallel/convergent amino acid substitutions were identified in mitochondrial OXPHOS genes of TST complex shrimps, which reflect functional convergence or similar genetic mechanisms of cave adaptation. The extensive occurrence of positive selection is suggestive of their essential role in adaptation to hypoxic anchialine environment, and further implying that TST complex shrimps might have acquired a finely capacity for energy metabolism. These results provided some new insights into the genetic basis of anchialine hypoxia adaptation.     

A new species of Typhlatya (Crustacea: Decapoda: Atyidae) from anchialine caves on the French Mediterranean coast

A new species of the thermophylic Tethyan relict prawn Typhlatya is described from two anchialine caves near Perpignan (southern France). The new species is closely related to a congener known only from a freshwater cave at Castellón (eastern Spain), about 400 km to the south-west, differing apparently only in the size and shape of the rostrum and the armature of the dactylus of the fifth pereiopod. Based on palaeogeographical evidence and assuming a sister-group relationship between both species, we suggest that their common ancestor could not be older than early Pliocene in age, and that it was already a stygobiont taxon adapted to live in shallow-water marine crevicular habitats. This ancestor would have vanished from the western Mediterranean after the cooling associated with the onset of northern Hemisphere glaciation, about 3 Mya, as documented for other Mediterranean marine taxa. Indeed, the genus is completely stygobiont and does not occur in fluvial environments. The Pyrenees represent a watershed boundary that eliminates the possibility of the derivation of one species from the other by active dispersal after establishment in continental waters.  © 2005 The Linnean Society of London, Zoological Journal of the Linnean Society , 2005, 144 , 387–414.     

The flora of the early Miocene Brandon Lignite, Vermont, USA. VIII. Caldesia (Alismataceae)

Caldesia, a genus of aquatic monocotyledons, is represented by four living species, which are widely distributed in the temperate and tropical Old World. The genus has an extensive Oligocene through Pleistocene fossil record in Eurasia. We survey the morphology of the extant and fossil fruits of the Alismataceae, and provide a detailed review of the morphology and anatomy of living and fossil Caldesia fruits. The latter exhibit substantial similarity, making the recognition of separate species on the basis of fruit morphology difficult. We erect the new species Caldesia brandoniana from the Early Miocene Brandon Lignite of Vermont primarily on the basis of its geographic isolation; careful revision of all fossil fruiting material of Caldesia might require placement of the Brandon specimens in a more inclusive form species. Together with leaves of Caldesia from the Miocene Clarkia flora of Idaho, this occurrence indicates that Caldesia was in the New World as recently as the Early Miocene.