Evolution of Nemertesia hydroids (Cnidaria: Hydrozoa,Plumulariidae) from the shallow and deep waters of the NE Atlantic and western Mediterranean

Moura, C. J., Cunha, M. R., Porteiro, F. M., Yesson, C. & Rogers, A. D. (2011) Evolution of Nemertesia hydroids (Cnidaria: Hydrozoa, Plumulariidae) from the shallow and deep waters of the NE Atlantic and Western Mediterranean. —Zoologica Scripta, 41, 79–96. Hydroid species from the genus Nemertesia develop some of the largest and most complex hydrozoan colonies. These colonies are abundant and ecologically important in both shallow and deep waters worldwide. Here, we analyse the systematics of most Nemertesia species from the NE Atlantic and Mediterranean using morphology and phylogenetic inferences of 16S rRNA haplotype data. Phylogeographical analysis revealed multiple movements of taxa to and from the Mediterranean after the Messinian salinity crisis through shallow and deep waters. The nominal species Nemertesia belini and Nemertesia antennina revealed multiple genetic lineages representing cryptic species diversity. Molecular phylogenetic evidence was supported by consistent phenotypic differences between lineages, and three and seven putative species were resolved within the N. belini and N. antennina complexes, respectively. Three putative species of the N. antennina complex found at different seamounts of Azores grouped in a clade clustered amongst the other four cryptic species present at neighbouring bathyal localities of the Gulf of Cadiz. These cryptic species, mostly from the deep sea, form a clade distantly related to the typical N. antennina from European coastal waters. Depth or environmental correlates of depth seem to influence the reproductive strategies of Nemertesia colonies and ultimately speciation. In particular, speciation of these hydroids must have been influenced by hydrography, habitat heterogeneity, isolation by distance and larval dispersal capacity. The deep sea is shown as an important environment in the generation and accumulation of lineages that may occasionally invade coastal waters in the NE Atlantic. Glacial cycles of cooling, along with changes in sea level, and eradication of some coastal faunas likely facilitated speciation and evolutionary transitions from deep to shallow waters.     

Phylogeography of a pan-Atlantic abyssal protobranch bivalve: implications for evolution in the Deep Atlantic

The deep sea is a vast and essentially continuous environment with few obvious barriers to gene flow. How populations diverge and new species form in this remote ecosystem is poorly understood. Phylogeographical analyses have begun to provide some insight into evolutionary processes at bathyal depths (<3000 m), but much less is known about evolution in the more extensive abyssal regions (>3000 m). Here, we quantify geographical and bathymetric patterns of genetic variation (16S rRNA mitochondrial gene) in the protobranch bivalve Ledella ultima, which is one of the most abundant abyssal protobranchs in the Atlantic with a broad bathymetric and geographical distribution. We found virtually no genetic divergence within basins and only modest divergence among eight Atlantic basins. Levels of population divergence among basins were related to geographical distance and were greater in the South Atlantic than in the North Atlantic. Ocean‐wide patterns of genetic variation indicate basin‐wide divergence that exceeds what others have found for abyssal organisms, but considerably less than bathyal protobranchs across similar geographical scales. Populations on either side of the Mid‐Atlantic Ridge in the North Atlantic differed, suggesting the Ridge might impede gene flow at abyssal depths. Our results indicate that abyssal populations might be quite large (cosmopolitan), exhibit only modest genetic structure and probably provide little potential for the formation of new species.     

In situ observation of chimaerid species in the Gorringe Bank: new distribution records for the north‐east Atlantic Ocean

In the framework of the R.V. Nautilus exploration programme, remotely operated vehicle (ROV) surveys were conducted at bathyal depths in the Gorringe Bank. Video transects revealed the presence of the chimaerids Chimaera opalescens and Hydrolagus affinis in the region. An identification key for the north‐east Atlantic species of the family Chimaeridae is proposed.     

Diversification of chemosymbiotic bivalves: origins and relationships of deeper water Lucinidae

Although species of the chemosymbiotic bivalve family Lucinidae are often diverse and abundant in shallow water habitats such as seagrass beds, new discoveries show that the family is equally speciose at slope and bathyal depths, particularly in the tropics, with records down to 2500 m. New molecular analyses including species from habitats down to 2000 m indicate that these cluster in four of seven recognized subfamilies: Leucosphaerinae, Myrteinae, Codakiinae, and Lucininae, with none of these comprising exclusively deep‐water species. Amongst the Leucosphaerinae, Alucinoma, Epidulcina, Dulcina, and Myrtina live mainly at depths greater than 200 m. Most Myrteinae inhabit water depths below 100 m, including Myrtea, Notomyrtea, Gloverina, and Elliptiolucina species. In the Codakinae, only the Lucinoma clade live in deep water; Codakia and Ctena clades are largely restricted to shallow water. Lucininae are the most speciose of the subfamilies but only four species analyzed, Troendleina sp., ‘Epicodakia’ falkandica, Bathyaustriella thionipta, and Cardiolucina quadrata, occur at depths greater than 200 m. Our results indicate that slope and bathyal lucinids have several and independent originations from different clades with a notable increased diversity in Leucosphaerinae and Myrteinae. Some of the deep‐water lucinids (e.g. Elliptiolucina, Dulcina, and Gloverina) have morphologies not seen in shallow water species, strongly suggesting speciation and radiation in these environments. By contrast, C. quadrata clusters with a group of shallow water congenors. Although not well investigated, offshore lucinids are usually found at sites of organic enrichment, including sunken vegetation, oxygen minimum zones, hydrocarbon seeps, and sedimented hydrothermal vents. The association of lucinids with hydrocarbon seeps is better understood and has been traced in the fossil record to the late Jurassic with successions of genera recognized; Lucinoma species are particularly prominent from the Oligocene to present day. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111 , 401–420.     

The tail tells the tale: taxonomy and biogeography of some Atlantic Chelidonura (Gastropoda: Cephalaspidea: Aglajidae) inferred from nuclear and mitochondrial gene data

Several western Atlantic species of Chelidonura have been described mainly based on differences in colour pattern. Sequence data from two mitochondrial [cytochrome oxidase I (COI), 16S] genes and a nuclear [histone 3 (H3)] gene have revealed that all colour forms previously recognized from across the Caribbean, Bahamas, and Bermuda belong to the same species, Chelidonura berolina. However, several specimens from the Bahamas are genetically and morphologically distinct and are herein described as a new species, Chelidonura normani sp. nov. Externally, C. normani can only be distinguished from C. berolina by the morphology of the posterior end of the body and not by colour pattern. Both C. berolina and C. normani are genetically and morphologically distinct from the eastern Atlantic species Chelidonura africana, but the split between C. berolina and C. normani predates the split between C. berolina and C. africana. All three species differ in their protoconch morphology, which suggests different developmental modes. Furthermore, all three species display a broad variation in colour pattern, which raises questions on the biological significance of colour in this group. The reasons for the divergence between C. berolina and C. normani remain unknown but could be related to the complex geological history of the western Atlantic. © 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 163 , 1077–1095.     

The family Myriotrochidae Théel (Echinodermata: Holothurioidea) in the deep northeast Atlantic Ocean

Recent sampling in the Rockall Trough, Porcupine Seabight and Porcupine Abyssal Plain, in the NE Atlantic, has yielded 200 specimens of apodous holothurians belonging to seven species of the family Myriotrochidae Théel from depths between 1000 and 4310 m. These include the type species of a new genus and two new species of existing genera. Parvotrochus belyaevi gen. et sp. nov . is described from some minute specimens from the Rockall Trough that possess both exceptionally small wheel-like deposits and numerous, large curved rods in the body wall and tentacles. Myriotrochus clarki sp. Nov . has affinities to M. vitreus (M. Sars) but shows differences in the shape of the plates of the calcareous ring and in having larger, frequently abnormally formed, wheels. Siniotrochus myriodontus sp. Nov . is similar to the type species of this genus, S. phoxus, Pawson, but differs in the arrangement of the teeth on the wheels. A single small specimen of Prototrochus Belyaev et Mironov from the Whittard Canyon, northern Bay of Biscay, is similar to P. minutus (Östergren), a species known only from the Sea of Japan, but differs in some characteristics of the wheels and tentacles. A new subspecies, P. zenkevitchi rockallensis subsp. nov. , is proposed for a form of P. zenkevitchi (Belyaev) that was the most common myriotrochid encountered. P. zenkevitchi was known previously only from a few localities in the Pacific and S Atlantic deep-sea trenches. Similarly, two species previously known only from the NE Pacific, Myriotrochus bathybius H. L. Clark and M. giganteus H. L. Clark, are also recorded from the N Atlantic for the first time. The synonymy of M. giganteus and M. sp. ex gr. macquariensis-giganteus Belyaev et Mironov is proposed. The greatest number both of specimens and species came from the areas most intensively sampled. The present records show that several species have world-wide distributions. The wide geographic separation of many records is the result of both poor sampling effort in the deep sea, particularly with fine-meshed gear, and the difficulties in sampling infaunal animals in the deep sea. Box core samples in the Rockall Trough suggest that the myriotrochids are more common in this area than would be supposed from epibenthic sledge data. Hence, myriotrochids may be more prevalent in the deep sea than previously thought.     

Biodiversity and distribution of the genus Gromia (Protista, Rhizaria) in the deep Weddell Sea (Southern Ocean)

We present a survey of morphospecies of Gromia, a genus of testate protists, from bathyal and abyssal depths in the Weddell Sea and adjacent areas of the Southern Ocean. This material represents the most extensive and diverse available collection of deep-sea gromiids so far recorded. The twelve species, nine of which are undescribed, are recognized on the basis of morphological criteria, including the test size and shape, the appearance and structure of the oral capsule, and the characteristics of the test wall. Most species have a single oral capsule, which is circular in plan view with a conical nipple-like shape in lateral view. One morphospecies has three oral capsules. The appearance and structure of the wall displays great variability among Gromia species, ranging from very delicate and transparent with highly reflective highlights to relatively thick with distinct patterns of ridges covering the surface. More often, however, differences in wall structure are more subtle. Most morphospecies were distributed at bathyal depths along the continental margin, but one was sampled at ~4,800 m, representing the first record of an abyssal gromiid. Concurrent with findings from other regions of the World’s oceans, the Weddell Sea gromiids were mostly found in surficial sediments in areas of elevated organic input, suggesting that deep-sea gromiids are likely to play an important role in carbon cycling in bathyal eutrophic regions through the ingestion and degradation of fresh organic matter.     

Nature and role of newly described symbiotic associations between a sea anemone and gastropods at bathyal depths in the NW Atlantic

The hormathiid sea anemone Allantactis parasitica was found living as an epibiont on numerous species of gastropods at depths of 725-1100 m along the continental slope of eastern Canada. The proportion of bathyal gastropods hosting 1-6 sea anemones reached 72.5% in a single trawl. Although A. parasitica was occasionally found on other substrata (i.e. empty shells, pebbles), laboratory trials confirmed that they preferably associate with living gastropods. Settlement of planula larvae occurred significantly more often on the shells of live bathyal gastropods than on all other substrata present in the tanks. Juvenile sea anemones (∼ 1 mm diameter) readily moved from the mud or other inert substrata onto shells of burrowed bathyal gastropods. Conversely, larvae, juveniles and adults of A. parasitica never associated with any shallow-water gastropods when given the opportunity. Trials exposing predatory sea stars (Leptasterias polaris) from shallow and bathyal depths to bathyal gastropods (Buccinum undatum) with epibiotic A. parasitica, and to asymbiotic bathyal and shallow-water B. undatum, revealed adaptive behaviours in both prey and predator. Shallow-water gastropods (devoid of epibionts) reacted defensively to L. polaris, whereas bathyal gastropods relied mostly on their epibionts to protect them, thus falling prey to L. polaris when the epibionts were removed. L. polaris from bathyal depths typically ignored symbiotic gastropods, but they consistently preyed on asymbiotic ones, while L. polaris from shallow areas initially attempted to prey on all gastropods, but learned to avoid those harbouring sea anemones. Furthermore, living as epibionts afforded sea anemones a means to escape one of their own predators, the sea star Crossaster papposus. The mutualistic relationship between hormathiid sea anemones and bathyal gastropods from the NW Atlantic may have evolved in response to predation pressure.     

A revision of the systematics of panther worms (Hofstenia spp., Acoela), with notes on color variation and genetic variation within the genus

Species of the genus Hofstenia are voracious predators and among the largest and most colorful of the Acoela. They are known from Japan, the Red Sea, the North Atlantic islands of Bermuda and the Bahamas, and the Caribbean and in a variety of habitats including the rocky intertidal, among Thalassia sea grass, on filamentous algae and decaying mangrove leaves. Certain color morphs associated with each of these habitats seem to have confused the taxonomy of the group. While brown-and-white banding and spotting patterns of Hofstenia miamia and Hofstenia giselae are distinctive for species associated with mangrove leaves and Thallasia sp. and are likely to be cryptic for these specific environments, we find some evidence to suggest that the coloration is mimicry of a nudibranch with aposematic coloration. The common plan in these patterns is one with three variously solid or spotted lighter cross bands on a dark background. Our examination of museum type material and live specimens of Hofstenia collected from Bahamas, Belize, Bermuda, and Panama revealed no internal morphological differences between the Hofstenia species occurring in the Caribbean. Similarly, our analyses of 18S and 28S molecular sequence data revealed no significant differences among specimens. Accordingly, we declare that Hofstenia giselae is a junior synonym of Hofstenia miamia, the three-banded panther worm. Electronic supplementary material The online version of this article (doi: ) contains supplementary material, which is available to authorized users. Handling editor: K. Martons     

New hyperbenthic species of Misophriopsis and Misophriella, first record of misophrioid copepods (Crustacea) from Antarctic waters

  Misophrioid copepods are reported for the first time from Antarctic waters. A species of each of the genera Misophriopsis and Misophriella is described from hyperbenthic layers of the continental shelf of the eastern Weddell Sea. The genus Misophria is also reported from these waters. Misophriopsis australis sp. nov. is the fifth representative of this widely distributed genus, previously reported from the North Atlantic, the China Sea, and both NW and NE quadrants of the Pacific Ocean. Misophriella schminkei sp. nov. is the second representative of the genus, known to date only from a single female caught in North Atlantic bathyal depths. Traces of subdivisions on antennary exopodal segments of the latter species suggest that the first segment may be a triple segment, while the second and terminal segments may be double segments. In addition, the mandibular exopod of this taxon indicates that a six-segmented ramus with setal formula 0, 1, 1, 1, 1, 2 may represent the ground pattern in Copepoda. The presence of parts of a cyclopinid copepod in the gut of M. schminkei sp. nov. indicates that this species may be carnivorous. Received: 12 November 1998 / Received in revised form: 26 July 1999 / Accepted: 27 July 1999     

Reproduction in marine invertebrates in “stable” environments: the deep sea model

Summary

Studies over the last 15 years have revealed that deep-sea benthic megainvertebrates show a variety of reproductive patterns that are adapted to the deep-sea, an environment in which the fauna occurs at low densities and resources are sparse. In the NE Atlantic the majority of species reproduce year round whilst a limited number of species reproduce on a seasonal basis believed to be entrained by the deposition of surface derived organic material on the deep-sea bed. A third pattern of rapid growth and early reproduction is found in a limited number of species that utilize unpredictable and ephemeral resources in the deep sea. Examination of the fertilization and behavioural biology of species from the bathyal depths suggest some species enhance fertilization success by forming pairs during their breeding season. However, the same concentration of sperm, as seen in shallow water invertebrates, is required for successful fertilization. At least one deep-sea species of echinoid requires high pressure for successful embryogenesis suggesting a depth-related segregation of deep-sea fauna. The origin of megafaunal populations of deep-sea invertebrates in the N. Atlantic is discussed in the light of these new data in relation to varying reproductive patterns and the environmental changes that have occurred during the last deglaciation.     

DNA barcoding of the northern Northeast Atlantic skates (Chondrichthyes,Rajiformes), with remarks on the widely distributed starry ray

The skate fauna in the northern Northeast (NE) Atlantic is poorly investigated, and misidentifications are common. Here, ‘DNA barcoding’ was used to analyse 105 specimens of 15 species previously reported from the area to investigate the occurrence of species. Of these 15 species, three were new to the region and confirmed with voucher specimens. Three previously reported taxa were not obtained from the study area, providing a total number of 12 skate species for the northern NE Atlantic. Only one specimen of the critically endangered Dipturus batis complex was found. It occurs frequently in the literature and commercial fisheries catch records, and we argue that the vast majority of these are misidentifications. Due to striking differences in Amblyraja radiata life history parameters across the North Atlantic, cryptic species diversity has previously been suspected. A total of 80 A. radiata cytochrome c oxidase subunit I sequences from across the North Atlantic were sampled, and the highest fixation index (F_ST) was found when maximising geographical distance (F_ST = 0.133). A lower index was found when grouped according to life history (F_ST = 0.067). These results are not strongly supportive for the occurrence of cryptic species.     

Complex Movements,Philopatry and Expanded Depth Range of a Severely Threatened Pelagic Shark,the Oceanic Whitetip (Carcharhinus longimanus) in the Western North Atlantic

Oceanic whitetip sharks (Carcharhinus longimanus) have recently been targeted for conservation in the western North Atlantic following severe declines in abundance. Pop-up satellite archival tags were applied to 11 mature oceanic whitetips (10 females, 1 male) near Cat Island in the central Bahamas 1–8 May 2011 to provide information about the horizontal and vertical movements of this species. Another large female was opportunistically tagged in the U.S. Exclusive Economic Zone (EEZ). Data from 1,563 total tracking days and 1,142,598 combined depth and temperature readings were obtained. Sharks tagged at Cat Island stayed within 500 km of the tagging site for ∼30 days before dispersing across 16,422 km² of the western North Atlantic. Maximum individual displacement from the tagging site ranged from 290–1940 km after times at liberty from 30–245 days, with individuals moving to several different destinations (the northern Lesser Antilles, the northern Bahamas, and north of the Windward Passage). Many sharks returned to The Bahamas after ∼150 days. Estimated residency times within The Bahamas EEZ, where longlining and commercial trade of sharks is illegal, were generally high (mean = 68.2% of time). Sharks spent 99.7% of their time shallower than 200 m and did not exhibit differences in day and night mean depths. There was a positive correlation between daily sea surface temperature and mean depth occupied, suggesting possible behavioral thermoregulation. All individuals made short duration (mean = 13.06 minutes) dives into the mesopelagic zone (down to 1082 m and 7.75°C), which occurred significantly more often at night. Ascent rates during these dives were significantly slower than descent rates, suggesting that these dives are for foraging. The sharks tracked appear to be most vulnerable to pelagic fishing gear deployed from 0–125 m depths, which they may encounter from June to October after leaving the protected waters of The Bahamas EEZ.     

Development and characterization of microsatellite markers for the endangered anchialine squat lobster Munidopsis polymorpha

Species of the genus Munidopsis are typically distributed in bathyal and abyssal zones, but the anchialine species Munidopsis polymorpha is an exception. It inhabits a volcanic tube on Lanzarote Island (Canary Islands, NE Atlantic) and is currently listed as endangered due to its highly restricted distribution and degree of endemism. Microsatellite loci were isolated from partial genomic libraries that had been enriched for AC, ACAG, GATA, AAAC and AAG repeat sequences. Eight loci were polymorphic in a sample of 24 individuals. The number of alleles per locus ranged from 2 to 4 with observed and expected heterozygosities ranging from 0.083 to 0.875 and from 0.080 to 0.681, respectively. These markers will be used to evaluate levels of genetic diversity and inbreeding, providing essential information for the development of a management and conservation strategy for this species.     

A molecular evaluation of the Liagoraceae sensu lato (Nemaliales,Rhodophyta) in Bermuda including Liagora nesophila sp. nov. and Yamadaella grassyi sp. nov.

We have undertaken a comprehensive, molecular‐assisted alpha‐taxonomic examination of the rhodophyte family Liagoraceae sensu lato, a group that has not previously been targeted for molecular studies in the western Atlantic. Sequence data from three molecular markers indicate that in Bermuda alone there are 10 species in nine different genera. These include the addition of three genera to the flora — Hommersandiophycus, Trichogloeopsis, and Yamadaella. Liagora pectinata, a species with a type locality in Bermuda, is phylogenetically allied with Indo‐Pacific species of Hommersandiophycus, and the species historically reported as L. ceranoides for the islands is morphologically and genetically distinct from that taxon, and is herein described as L. nesophila sp. nov. Molecular sequence data have also uncovered the Indo‐Pacific L. mannarensis in Bermuda, a long‐distance new western Atlantic record. DNA sequences of Trichogloeopsis pedicellata from the type locality (Bahamas) match with local specimens demonstrating its presence in Bermuda. We described Yamadaella grassyi sp. nov. from Bermuda, a species phylogenetically and morphologically distinct from the generitype, Y. caenomyce of the Indo‐Pacific. Our data also indicated a single species each of Ganonema, Gloiocallis, Helminthocladia, Titanophycus, and Trichogloea in the flora.     

An eddy,a wake and a plume: controls on bathyal foraminifera around Tobago,western tropical Atlantic Ocean

Oceanic islands in the paths of currents induce the development of wakes and stationary eddies. The situation to the lee of Tobago, western tropical Atlantic Ocean, is further complicated by the occurrence of the seasonally variable, hypopycnal Orinoco plume. Here we investigate the impact of the combined plume, wake and eddy on bathyal benthic foraminifera to the NW of Tobago. Three surface sediment samples were recovered from around each of five well-sites to the NW of Tobago, three of the sites (Warap-A, Cassra-A and Cassra-CC) being at upper bathyal depths and two (Bene-1, Sancoche-1) at middle bathyal depths. Warap-A, Cassra-A, Cassra-CC and Bene-1 form a transect along the northern side of the leeward wake, while the other two sites are in the vicinity of the stationary eddy. The samples obtained around Sancoche-1 were taken north of the wake. These were supplemented by samples from four 80-cm piston cores from upper bathyal and outer neritic depths sampled at ~ 10 cm intervals. Benthic foraminifera reveal different biofacies at upper (Warap-A, Cassra-A, Cassra-CC) and middle (Bene-1, Sancoche-1) bathyal depths. The upper bathyal biofacies is dominated by Cassidulina curvata and the middle bathyal biofacies contains abundant Uvigerina hispidocostata, both of which are indicative of a high nutrient flux. The presence of Martinottiella communis and M. pallida at Warap-A indicate that pore waters are low in dissolved oxygen in the immediate lee of the island. Percentages of the fauna as serial tests indicated decreasing current velocities with increasing depth, as confirmed by the high abundance of Cibicides ex gr. aknerianus in the shallowest water core. Upper bathyal bottom-current strength was at its lowest in the immediate lee of the island. Species indicative of a perennial nutrient flux were more abundant to the NW, where the interaction of the plume and eddy appears to concentrate nutrients. The short cores, each from a different biofacies, indicate that these environmental conditions have been in place for at least the later Holocene. The most northerly, upper bathyal core presented a stable community structure with low assemblage turnover, while two cores taken farther south (upper bathyal and outer neritic) had an expansive structure with high assemblage turnover. These data raise the possibility of using benthic foraminifera to track the positions of the plume, core and eddy throughout the later Neogene.     

Osmotic and ionic hemolymph concentrations of bathyal and abyssal amphipods of Lake Baikal (Siberia) in relation to water depth

We studied the adaptive variations of the hemolymph concentrations in relation to water depth and pressure using deep-dwelling amphipods from Lake Baikal. Hemolymph osmolality was determined in six bathyal and abyssal species immediately after capture when values come closest to the habitat concentrations. In three species, hemolymph osmolalities correlated positively with depth of capture. Prevalent ions in the hemolymph are sodium and chloride. Lactate, our indicator for capture stress, was highest after trawling (2–6 mM) and lowest after retrieval from cages (0–0.6 mM). Acclimation to different pressure was studied by exposing the specimens to different water depths over several days. Hemolymph concentrations did not change after acclimation to surface pressure in the sublittoral Acanthogammarus albus, a native also to shallow water, but decreased by 30–80 mosmol/kg H₂O in the bathyal and abyssal species Acanthogammarus grewingki, Acanthogammarus reicherti, and Parapallasea lagowskii. Similarly, hemolymph osmolality decreased in A. reicherti and P. lagowskii originating from deep water, when acclimated to reduced water depth, and, in A. reicherti hemolymph osmolality reached its original high value when returned to the depth of capture. Higher hemolymph osmolalities and NaCl concentrations, demonstrated here for the first time, may provide selective advantages to abyssal species. Accepted: 24 August 2000