Diversity of deep-sea echinoderms from Costa Rica

Echinoderms are a highly diverse group and one of the most conspicuous in the deep sea, playing ecological key roles. We present a review about the history of expeditions and studies on deep-sea echinoderms in Costa Rica, including an updated list of species. We used literature and information gathered from the databases of the California Academy of Sciences, the Benthic Invertebrate Collection of the Scripps Institution of Oceanography, the National Museum of Natural History, the Museum of Comparative Zoology and the Museo de Zoología from the Universidad de Costa Rica. A total of 124 taxa (76 confirmed species) have been collected from the Costa Rican deep sea, 112 found in the Pacific Ocean, 13 in the Caribbean Sea, and one species shared between the two basins. We report 22 new records for the Eastern Tropical Pacific, 46 for Central American waters, and 58 for Costa Rica. The most specious group was Ophiuroidea with 37 taxa, followed by Holothuroidea (34 taxa), Asteroidea (23 taxa), Echinoidea (17 taxa), and Crinoidea (11 taxa). The highest number of species (64) was found between 800 m and 1200 m depth. Only two species were found deeper than 3200 m. Further efforts on identification will be required for a better comprehension of the diversity of deep-sea echinoderms. Limited research has been done regarding the biology and ecology of deep-sea echinoderms in Costa Rica, so additional approaches will be necessary to understand their ecological functions.UCR::Vicerrectoría de Investigación::Unidades de Investigación::Ciencias Básicas::Centro de Investigación en Ciencias del Mar y Limnología (CIMAR)UCR::Vicerrectoría de Investigación::Unidades de Investigación::Ciencias Básicas::Centro de Investigación en Biodiversidad y Ecología Tropical (CIBET)UCR::Vicerrectoría de Docencia::Ciencias Básicas::Facultad de Ciencias::Escuela de Biologí

The Holothurioidea (Echinodermata) collected during the Tyro Mauritania-II expedition 1988

During the Tyro Mauritania-II expedition (5-21.vi.1988) 15 holothurian species were collected between 19 and 1,900 m depth. Twelve species are new to the fauna of Mauritania, including Paracucumaria deridderae spec. nov. Mauritania represents the southern distribution limit of four species also known from Europe, and the northern distribution limit of five species also known from southern Africa

Trophodynamics on mid-ocean ridges

PhD ThesisThe global mid-ocean ridge (MOR) system is ~60 000 km long and accounts for 9% of the seafloor. Deep-sea organisms living on MOR have two potential energy sources; chemosynthesis and the downward flux of photosynthetic organic matter. This study examines the trophodynamics of benthic fauna collected from non-vent sites north and south of the Charlie-Gibb Fracture Zone (CGFZ) on the Mid-Atlantic Ridge (MAR) and hydrothermal vents fields (E2 and E9) on the East Scotia Ridge (ESR) using stable isotopes of carbon (δ13C), nitrogen (δ15N) and sulphur (δ34S). δ13C and δ34S values revealed the MAR benthos was sustained by photosynthetic primary production and no chemosynthetic food source was detected. δ15N values of benthic invertebrates were lower than the surficial sediments at the southern site but this did not occur at the northern site. Benthic invertebrates appeared to comprise a separate food chain to bentho-pelagic fishes and crustaceans but size-based trends in δ13C and δ15N revealed at certain life history stages bentho-pelagic fishes may consume benthic fauna. Size-based trends in δ13C and δ15N trends varied spatially and temporally in some bentho-pelagic fishes, which suggested differences in feeding plasticity among the species. Spatial differences among sites were observed in δ13C, δ15N and δ34S of the ESR vent fauna. These were thought to reflect differences in the vent fluid chemistry, vent derived carbon fixation pathways and incorporation of photosynthetic organic matter into the vent system depending on the species and the magnitude of the difference among sites. Size and sex were important determinants of intra-population variability in stable isotope values of three species of vent fauna but this was not consistent among sites. Abstract ii The present study revealed the importance of undertaking a tri-isotope approach to deep-sea trophic studies in order to elucidate production sources and at different sizes deep-sea organisms can link different trophic pathways.The work was funded by the Natural Environment Research Council and consisted of a studentship NE/F010664/1; sample analysis via Life Sciences Mass Spectrometry Facility grants EK127-10/08, EK150-12/09 and LSMFBRIS043_04/10_R_09/10; ECOMAR consortium grant NR/C512961/1; and ChEsSo consortium grant NE/DO1249X/1. I’m very grateful to my parents and sister for all the love and support they have given me over the years. Finally, I would like to thank Charlotte. Thank you for your patience, support, encouragement, cups of tea, cooked meals and constantly being there for me whether I was at sea, home or when I thought the PhD was crumbling around me. I could neve

A deep life: The application of stable isotopes to understand deep-sea environments with a focus on latitudinal gradients

The deep-sea, defined as the area 200 m below the surface, is facing emerging chemical, physical and biological stressors. Currently, very little is known regarding deep-sea ecosystems both globally and in the Arctic. In this thesis I undertook a literature review on the current understanding of global deep-sea ecosystems through the use of stable isotopes. Specifically, I synthesized the available literature on spatial variation, energy pathways, depth, temporal variation, feeding behaviour, niche, trophic position and body size isotopic trends. This thesis then presents a case study examining the isotopic niche of five teleost and two decapod species within Arctic deep-sea food webs across the localized latitudinal gradient of Baffin Island. Spatial variation in isotopic niche was quantified using 13C and 15N for seven deep-sea species at three locations on Baffin Island, Nunavut to determine whether the “Latitudinal Niche Breadth Hypothesis” which states that niche breadth should increase with latitude holds true in the Arctic. Overall, isotopic patterns in global deep-sea ecosystem are variable; consistent trends are not observed across all taxa and habitats. It was concluded that niche breadth did not consistently increase with latitude in the eastern Canadian Arctic; localized conditions (e.g. sea ice, temperature) and individual condition (e.g. hepatosomatic index) may contribute more to a species’ niche than latitude. Overall, this thesis improves our understanding of deep-sea ecosystems globally, contributes baseline data for future monitoring, and by investigating multiple species and locations it will provide input on how climate change may impact Arctic food web diversity, energy dynamics and ecosystem structure to aid in sustainable fishery development

Echinoderm Biodiversity and Biogeography in Oceanic Islands: the Azores as a case study

Oceanic Islands are natural laboratories for the study of the processes and patterns of dispersion, colonization and ultimately of the appearance of new species. In the Northeast Atlantic, the archipelago of the Azores meets all the requirements to be considered one of the most isolated oceanic island systems. In general terms, the Azorean biota, as other oceanic systems, derives from dispersal chance events. For shallow-water marine benthic organisms, the main mechanisms to overcome the isolation by distance are rafting by non-planktonic life stages and through planktonic larval stages, both of which rely heavily on sea-surface currents to travel. However, and in spite of being under the influence of the western-intensified Gulf Current, the Azorean biota shows an opposite trend, being predominantly derived from the NE Atlantic and the Mediterranean. This apparent paradox has startled many marine biogeographers, who search for answers in the present-day faunal patterns together with those reconstructed through the past geological history of the archipelago. The present study attempts to further contribute to the knowledge of the marine fauna of the Azores, and its biogeographical relationships, using the echinoderms as a model. This animal phylum encloses a diverse group of strictly marine invertebrates found at all latitudes and depths. Furthermore, the echinoderms form one of the most conspicuous elements of both shallow- and deep-sea fauna in the Azores, and both in extant waters and among the fossiliferous outcrops of Santa Maria (37°N23’ 24°45’W), the oldest island in the archipelago. Thus, for a clear biogeographical background it was necessary to construct an updated catalogue of both local extant and fossil echinoderm fauna. During the International Workshops ‘Palaeontology in Atlantic Islands’, held in Santa Maria Island between 2002-2013, new material was collected from Lower Pliocene and Pleistocene deposits. The early Pliocene beds encompass the following taxa: Eucidaris tribuloides, Echinoneus cf. cyclostomus, Clypeaster altus, Echinocyamus pusillus, Echinocardium sp. 1, Echinocardium sp. 2, Schizobrissus sp. and undetermined spatangoids. The Pleistocene outcrops (MISS 5e) included three regular echinoid species, Sphaerechinus granularis, Arbacia lixula and Paracentrotus lividus. The small irregular echinoid Echinocyamus pusillus was also present in the Azorean Pleistocene fauna, a species common as well in the extant coasts of the archipelago. The presence of tropical taxa in the early Pliocene sediments clearly contrasts with the warm temperate taxa found in the Pleistocene and present coasts of the Azores. Updated faunal lists are fundamental in biodiversity and biogeographical studies. Arbaciella elegans is a small cryptic echinoid species that was believed to have a large geographical range from the tropical Atlantic waters of Central Africa to the northern shores of the Azores, Canaries, Northwest Africa and Mediterranean Sea. However, and unlike the Central African material, individuals from the warm temperate waters present a uniform dark color. A morphological and genetic characterization of specimens from the Azores shows that the dark Arbaciella phenotype represents in fact juvenile stages of Arbacia lixula, which implies that A. elegans is circumscribed to the tropical African waters from where it was first described. This study emphasizes the difficulty of constructing faunal lists mirroring true distributions of species or local biodiversity, when rare or cryptic species are involved. The Faculty of Sciencie and Tecnology (University of the Azores), houses hundreds of echinoderm specimens collected over more than 20 years of activity by the former Department of Biology. Three young specimens of the Mediterranean sea star Sclerasterias richardi (Perrier, in Milne-Edwards, 1882), a species previously not known to the Azores, were found among the echinoderm material. These animals were dredged off the south coast of São Miguel Island, at 135 m depth. Sclerasterias richardi is one of two sea star species known to reproduce asexually through fission in the Azores, the other being the shallow-water Coscinasterias tenuispina (Lamarck, 1816). However, S. richardi, though a shelf species, lives at much deeper waters than the latter. S. richardi is also capable of producing long-lived planktotrophic larvae with high dispersal potential to reach remote areas such as the Azores. The presence of S. richardi in Azorean waters in an otherwise thoroughly investigated area does not necessarily imply a recent arrival, as the depths in consideration (80-700 m) are also the least studied in the archipelago. The review of the extant echinoderm fauna of the Azores, based on the related bibliography that has been accumulating over 150 years, complemented with the construction of an important local echinoderm reference collection in the University of the Azores, resulted in a critical reassessment of this significant component of the Azorean marine fauna. Herein are reported 172 species of echinoderms (6 crinoids, 55 ophiuroids, 45 asteroids, 36 holothuroids and 30 echinoids) to the archipelago, most of them inhabiting deep-waters. Although 65 species could be classified as shelf species (840 m) appear to be restricted to the Azorean waters. Though relatively poorer in number of species, the Azores show similar general trends to what is observed in other Macaronesian archipelagos (i.e. Madeira, Canaries and Selvagens): lack of endemic species, dominance of echinoderm fauna generally associated with rocky shores and species capable of producing planktonic feeding larvae. The relatively low echinoderm diversity could be attributed to the archipelago remoteness, the northern geographical position and to other local features attributed to their relative young volcanic age (e.g., lower habitat diversity). The echinoderm fauna of the Azores encompasses several edible species, though none known to be traditionally harvested. In recent years, fisheries targeting holothurian species have developed dramatically in several European and North African countries, and two of the most common sea-cumber species in the Azores, Holothuria mammata and H. sanctori, are now being commercially harvested in the Northeast Atlantic and in the Mediterranean Sea. The identification of Holothuria species tends to be difficult and time-consuming, and in many cases requires experienced taxonomists. Conversely, the use of PCR-RFLPs to rapidly and inexpensively identify species with no need for taxonomical or genetic expertise could prove a valuable asset. The present work introduces a simple and fast method, using restriction nuclease Sau3AI on 16S rRNA fragments. A simple non-destructive DNA sampling is also presented, using tube feet or oral tentacles, to be applied in genetic studies. The updated faunal list of the echinoderms of the Azores was combined with those from the other areas in an updated distributional catalogue of the shallow-water echinoderms (≤200 m depth) from the North and Central Atlantic, and the Mediterranean Sea, providing the basic framework for the analysis of biodiversity patterns and the construction of a biogeographical model. A total of 891 species belonging to 341 genera of shallow-water echinoderms are presently recorded in the studied areas. The tropical West Atlantic was by far the most biodiverse region (483 species, 210 of which were endemic). The Mediterranean Sea did not emerge as a biodiversity hotspot, revealing similar biodiversity rates as the neighbouring regions of Iberian and NW Africa, but presented significant endemism rate. Among the insular systems, Canaries presented the highest echinoderm biodiversity with 85 species, followed by Cabo Verde with 76. A positive correlation between latitude and the species’ depth range was detected, confirming the Rapoport’s latitudinal gradient. The most common larval development was planktotrophic (119 species), followed by the lecithotrophic (71 species) and aplanktonic (47 species). The relative representation of lecithotrophic and aplanktonic larval development increased towards high latitude areas and decreased as species geographical range increased. Also, the asexual reproduction decreased towards high latitude colder areas and this reduction was correlated with the relative increase of aplanktonic larval mode of development in the same areas. Endemic species were particularly numerous among sediment-associated habitats and broadly distributed species showed no preference for either soft or hard bottoms. Most areas showed a natural decrease of shared species with increasing geographical distance and this was particularly evident in oceanic systems. In these, faunal affinities tended to be related with the nearest continental shores, regardless of the prevailing sea-surface currents. In general, echinoderms proved to be good models for testing biodiversity and biogeographical patterns, though significant gaps were found on the available information

Post-larval development in deep-sea echinoderms

The post-larval phase is an essential period in the life history of marine invertebrates; vulnerable to high mortality, it ultimately influences the distribution and abundance of adult populations. The post metamorphic ontogenesis of thirty species of deep-sea echinoderms, belonging to three classes (Ophiuroidea, Asteroidea and Echinoidea), is described using scanning electron microscopy. The life history of Ophiocten gracilis is also examined as a case study for future research on post-larval organisms. The analysis of development in ophiuroids reveals that species can be identified from a very early post metamorphic stage, even in congeneric species, contrary to the findings of other authors. The ontogeny of homologous structures is similar within related groups, but may give rise to different adult structures indifferent taxa. The mouth papillae within the ophiurids are serially homologous, originating from the jaw, but the fourth mouth papilla may have a different origin. In the families Ophiactidae, Ophiacanthidae and Amphilepididae examined, the mouth papillae have different origins, as, for instance, the adoral shieldspine or tentacle scale. Data on the post-larval development of Ophiura affinis suggest that this species is more closely related to the genus Ophiocten and a change in the generic status is proposed. Ophiocten gracilis is a bathyal brittle star occurring on both sides of the North Atlantic and its life history is studied in the eastern side of the North Atlantic. In this area, O. gracilis spawns in February/March of each year producing a large number of eggs. Fecundity is estimated to be around 40,000 eggs/ind, with the population of the Hebridean Slope being able to produce probably up to 16 million eggs/m2. Post-larvae start settling in May and numbers settling reached over 3,200 post-larvae/m2. The settling speed of post-larvae in the water column is estimated to be around 500 m/day, settling faster in warmer than colder water. Settling speeds appear to be similar for post-larvae ranging from 0.6 to 0.9 mm in disk diameter. Size at settlement is around 0.6 mm in disk diameter and 5-6 arm segments. The settlement of post-larval O. gracilis on the bottom of the Hebridean Slope also represented a considerable fraction of the particulate organic carbon (POC) flux in the area, reaching over 7% of the total daily flux. This is likely to have a considerable impact in the benthic community as competition and predation and as an additional food source for demersal and benthic organisms. The occurrence of post-larvae of O. gracilis in sediment traps also represented a large problem for POC flux measurements, with ophiuroids consuming part of the flux. In future works with sediment traps, such errors must be taken into account and ophiuroids must be included in the total POC flux. The deep-sea juvenile asteroids of the NE Atlantic could be distinguished to species level from a very early stage of development. The ontogenesis of Porcellanaster ceruleus shows that this species is likely to undergo a shift in habitat and diet during the juvenile phase. This is evidenced by the appearance of the epiproctal cone, the changing of the furrow and apical spines, the early development of the cribriform organ adjacent to the madreporite and the appearance of sediment in the stomach. P. ceruleus is probably a predator on meiofauna and small macrofaunal organisms during the early stages of life, changing to a burrowed life style ingesting sediment particles. Most juvenile sea stars analysed during the present study showed wider bathymetric distribution than their adult counterparts, suggesting that events occurring during the early stages of life are important for the maintenance of the local population structure and diversity in the deep NE Atlantic.The post-metamorphic development of three deep-sea spatangoid echinoids is very similar, but the morphology and formation of fascioles facilitate the distinction of the species examined. Whereas in Hemiaster expergitus and Spatangus raschi the fascioles present in the post-larvae develop to form the adult fascioles, in Brissopsis lyrifera post-larvae there is a juvenile fasciole, which disappears during ontogenesis giving way to the adult fascioles. The function of the juvenile fasciole is unknown in B.lyrifera. The development of the periproct in all spatangoids examined is similar to that described by other authors, with the periproct being initially endocyclic and migrating towards the rear of the animal as development progresses. Post-larvae of the genus Echinus could not be separated into different species, which may be linked to the recent diversification of the genus in the North Atlantic. The widespread settlement of echinoderm post-larvae reported in the present thesis and in other works is thought to have been very important for the colonization of the deep-sea through the supply of stages to deeper areas and selection of pressure adapted animals and subsequent speciation

Seasonality and selectivity in the feeding ecology and reproductive biology of deep-sea bathyal holothurians

Chlorophyll and carotenoid pigments were determined from the gut sediments of five species of bathyal holothurian in the NE Atlantic, sampled shortly after the spring/summer phytoplankton bloom in 2001 and prior to the spring bloom in 2002. Three species, Laetmogone violacea, Paroriza pallens and Bathyplotes natans, sampled within a similar depth range (900–1100 m) in the summer of 2001 showed significant differences in their chlorophyll and carotenoid pigment concentrations. This suggests they may select for slightly different components from the available food resource. Four species sampled in early spring 2002, Laetmogone violacea, Paroriza pallens, Benthogone rosea and Benthothuria funebris, also had significant differences in their pigment concentrations. These species were sampled over a wider depth range (1000–3100 m) showing a bathymetric trend in pigment concentrations. There was a distinct seasonal change in the composition and concentration of the pigments, linked to a reduction in the availability of fresh organic material during autumn and winter periods.Ovarian tissue was also examined. The carotenoid pigments found in the ovary also occurred in the OM ingested by the holothurians. The dominant gonadal carotenoid pigments were beta-carotene, echinenone and zeaxanthin. The potential for using these carotenoids to gain a competitive advantage through selectivity of chlorophyll and carotenoid pigment biomarkers are discussed in relation to competition for food resources by deposit-feeders. The results were also compared with selectivity in abyssal species

Deep-sea biology food for thought? : examining dietary selection and resource allocation in deep-sea holothurians

This study examined the complex link between surface production and the feeding ecology of a range of holothurian species from both abyssal and bathyal depths on the PAP and PSB over 3 seasonal periods from Summer 2001 to Autumn 2002 using a range of biochemical techniques and novel experimental work. The chlorophyll and carotenoid pigments taken from the gut contents of over 14 holothurian species showed significant between-species difference in the concentration, and to some extent composition of pigment.  Individual species were shown to have subtly different preferences for different pigment biomarkers, derived from different types of OM contained within the seafloor sediment.  One of the most noticeable differences occurred in Amperima rosea.  The study showed that A. rosea had a consistently higher pigment concentration than all other abyssal species during all the sampling periods. The pigment composition was also significantly different, with large concentrations of zeaxanthin, echinenone and β-carotene.  Examining the remaining abyssal species, showed that A. rosea was able to feed preferentially upon the labile fractions of the sediment, leaving the more refractory breakdown products for the other species to utilise. Trends within bathyal species were somewhat different. Most bathyal species had similar pigment compositions, but there were significant differences in overall pigment concentration.  As species were sampled with increasing depth down the continental slope, the pigment concentration found within the gut contents of different holothurian species increased, with highest concentrations in Benthothuria funebris, sampled from 3000m. The pigment concentrations of both bathyal and abyssal holothurians showed marked seasonal patterns.  In periods during, and directly after, spring blooms, the concentration of pigments within gut contents was an order of magnitude higher than in pre-bloom periods. To determine how holothurians assimilate and utilise labile OM, gonadal material from bathyal and abyssal species was examined.  From a suite over 10 pigments ingested, only a small number were found within the gonad, most notably echinenone and β-carotene.  These labile carotenoids were concentrated in the gonad by an order of magnitude when compared with levels in gut contents.  These carotenoids are used in aquaculture to stimulate increased egg production and growth.  The high level of these carotenoids in deep-sea holothurians suggests they rely upon OM flux to provide key biochemical components crucial for reproduction and development. Using a fatty acid biomarker approach, a similar seasonal pattern in the dietary requirement of holothurians was shown. All species selected polyunsaturated fatty acids (PUFAs) in preference to other groups of lipid.  The highest levels of PUFA coincided with the arrival of OM associated with the spring bloom, much in the same way as pigment concentrations, especially labile carotenoids also increased.</p

Deep-sea Holothuroidea off Mauritania

Among invertebrates, echinoderms are one of the main benthic taxa, especially in deep bottoms, where they constitute the most important group of mobile epifauna (Gage and Tyler, 1991). In addition, holothurians are one of the taxa dominating epibenthic communities in different North Atlantic basins (Billet, 1991), where they can form dense aggregations. Despite the large literature on Atlantic echinoderms, the knowledge of this group in Northwest African waters primarily comes from the pioneering oceanographic expeditions carried out from late nineteenth century to mid twentieth century. However, the current knowledge of holothurians in Mauritanian waters is scarce, and only the works of Koehler and Vaney (1906), Hérouard (1929) and Massin (1993) were focused in this group and mainly on the fauna of the northern continental shelf. This is a taxonomic and ecological study of the holothurians collected during the four multidisciplinary Spanish – Mauritanian surveys (Maurit) carried out from 2007 to 2010 on board R/V Vizconde de Eza in Mauritanian EEZ waters, between Cape Blanc (21ºN) and the Senegalese border (16ºN). A total of 291 stations were sampled between 80 and 2000 m depth, following a stratified random sampling methodology with and using a Lofoten commercial trawl (17.7 m horizontal opening, 5.5 m vertical opening and 35 mm mesh in the cod-end). The holothurians collected in each trawl were sorted to morphospecies level, counted and weighed to obtain quantitative data on their abundance and biomass. Each specimen was photographed and a reference collection was preserved in 70% alcohol for further identification in the laboratory. The identification methodology included the study of the external and internal morphology by dissection and the microscopic study of the endoskeletal calcareous deposits. Quantitative data (numerical abundance and biomass) collected during Maurit-0811, were standardized to 0.1 km2 and their respective matrices were calculated to enable an analysis of similarity between stations using the Bray Curtis index. Statistical treatment was performed using PRIMER software package v.6. During the four cruises a total of 193,791 holothurians were collected in 128 of the 291 sampled stations, belonging to 15 species and 9 families. In terms of number of species, Synallactidae showed the highest specific richness (6 species), followed by Laetmogonidae (2 species). The others families were represented by only 1 species. Enypniastes eximia Theel, 1882, the only representative of the family Pelagothuriidae, showed the greatest occurrence (52%) and was also the dominant species, both in numbers and biomass. Paelopatides grisea Perrier, 1898 and Benthothuria funebris Perrier, 1898 were collected in about 40% of the stations and, due to their big size, they significantly contributed to the total biomass despite their low numerical abundance. The multidimensional scaling (MDS) and the dendrogram resulting from the multivariate analysis applied to biomass matrix clearly separated stations located in the deep-shell and upper slope (<300 m) from those located at greater depths along the continental slope. The dendrogram evidenced five groups, two of them corresponding to shelf and upper slope stations (80–300 m) and the others including stations beyond 1000 m depth. Holothurians were almost absent between 300 and 1000 m in Mauritanian slope, which is in agreement with the results obtained by Billet (1991) in Porcupine Seabight (North Atlantic), where the abundance of holothurians was low in the break upper slope area (200 to 1000 m) but clearly increased beyond. References Billet, D.S.M. 1991. Oceanography and Marine Biology: An Annual Review, 29: 259-317. Gage, J. D. & Tyler, P. A. 1991. Cambridge University Press, 504 pp. Hérouard, E. 1902. Résultats des Campagnes Scientifiques Prince Albert I de Monaco, 21: 1-83. Koehler, R. & Vaney, C. 1906. Act. Soc. Linn. Bordeaux, 60: 59-67. Massin, C. 1993. Zoologische Mededelingen, 67:397-429.MAVA (contract 12/87 AO C4/2012