Abyssal Holothurian Research Articles

Deconvolving feeding niches and strategies of abyssal holothurians from their stable isotope, amino acid, and fatty acid composition

Deconvolving feeding niches and strategies of abyssal holothurians from their stable isotope, amino acid, and fatty acid composition

Long-term and seasonal changes in the life-history biology of the abyssal holothurian Pseudostichopus aemulatus from the Porcupine Abyssal Plain (North-East Atlantic)

Long-term interannual variations in the benthic community structure are well-known from abyssal plains in the North Atlantic and North Pacific, where rapid responses to changes in the environment by first-order opportunists modify overall species composition. To increase our knowledge of the long-term variations of deep-sea benthic communities in the North-East Atlantic, we studied the response of a second-order opportunist echinoderm, the holothurian Pseudostichopus aemulatus, before, during and after the “Amperima Event” – a four-year episode (1996–1999) where the first-order opportunistic holothurian, Amperima rosea, increased dramatically in density. We used a collection of 14 sampling times of deep-sea community assemblage over a sixteen-year period to understand the temporal variation (i.e., interannual and seasonal) in population structure (i.e., density and individual sizes) and reproduction (i.e., mean oocyte sizes, sex ratios, gonadal indices, and fecundity) in P. aemulatus. Samples were collected from the Porcupine Abyssal Plain (PAP) in the NE Atlantic Ocean at a depth of ca. 4850 m between 1989 and 2005 with a semi-balloon otter trawl (OTSB14) and an epibenthic sledge (BN1.5/C) at varying seasons. We measured individual body size, dissected organisms to prepare histological slides of their gonads, and measured the Feret oocyte diameter in females. We found changes in the life-history biology of P. aemulatus during the “Amperima Event”. Population density increased gradually from September 1997 until April 1999, when P. aemulatus reached a peak in density coinciding with the smallest mean body size observed (1998 and 1999) suggesting recruitment of juveniles. In 1997, before these changes in population structure, mean oocyte sizes were at their largest, suggesting a strong reproductive effort with individuals either preparing to spawn or spawning. This reproductive effort was minimal in the years after 1999, when we found the largest proportions of previtellogenic oocytes in individuals that were probably allocating their energy into growth rather than reproduction given their smaller size. The presence of gametes of all sizes across seasons and a broad range of individual sizes in various sampling times suggests no seasonal reproductive patterns. We suggest that feeding guild differences between various holothurian species explain the diverse life-history responses observed among holothurians competing for resources in a food-poor environment.

Possible links between holothurian lipid compositions and differences in organic matter (OM) supply at the western Pacific abyssal plains

Deep-sea benthic communities depend on the export of organic matter (OM) from the surface ocean. However, the effects of the pelagic-benthic coupling and the specific link between changing seasonal OM inputs and physiological changes of the mega-benthic community remain unclear. In this study, we identified differences in OM quality and quantity at two abyssal seafloor sites in the western Pacific Ocean and noted possible links between overlying primary production and the lipid composition of several deep-sea holothurian species. Phytopigment concentrations of the surface sediment were up to 16-times greater at the high productivity area (39°N) than at the oligotrophic area (1°N). Total carbohydrate and protein concentrations were also significantly higher at 39°N than 1°N, although to a lesser extent than for phytopigments. Holothurian abundances were almost 40 times higher at 39°N than 1° N. Significant differences were detected in the fatty acid (FA) compositions of the holothurian tissues in terms of proportions of the main food source indices (phytoplankton, zooplankton and bacterial FA), suggesting different food sources in the two areas. Phytodetritus and bacteria were the most dominant dietary sources at 39°N and 1°N, respectively. Stable carbon and nitrogen isotopic compositions did not contradict the FA data indicating that holothurians fed on both phytodetritus and bacteria from the sediments.Overall, our results show that high densities of abyssal holothurians at 39°N is linked with the high quality of the sedimentary OM associated with the net primary production at the surface. Further, the differences in phytodetritus inputs may lead to a different lipid composition as a consequence of different feeding habits, although there may be some other mechanisms behind. This study provides fundamental knowledge on lipid compositions of abyssal holothurians in relation to oceanic settings, thus improves our understanding of the ecosystem functioning in abyssal plains.

Metabolic rates are significantly lower in abyssal Holothuroidea than in shallow-water Holothuroidea.

Recent analyses of metabolic rates in fishes, echinoderms, crustaceans and cephalopods have concluded that bathymetric declines in temperature- and mass-normalized metabolic rate do not result from resource-limitation (e.g. oxygen or food/chemical energy), decreasing temperature or increasing hydrostatic pressure. Instead, based on contrasting bathymetric patterns reported in the metabolic rates of visual and non-visual taxa, declining metabolic rate with depth is proposed to result from relaxation of selection for high locomotory capacity in visual predators as light diminishes. Here, we present metabolic rates of Holothuroidea, a non-visual benthic and benthopelagic echinoderm class, determined in situ at abyssal depths (greater than 4000 m depth). Mean temperature- and mass-normalized metabolic rate did not differ significantly between shallow-water (less than 200 m depth) and bathyal (200–4000 m depth) holothurians, but was significantly lower in abyssal (greater than 4000 m depth) holothurians than in shallow-water holothurians. These results support the dominance of the visual interactions hypothesis at bathyal depths, but indicate that ecological or evolutionary pressures other than biotic visual interactions contribute to bathymetric variation in holothurian metabolic rates. Multiple nonlinear regression assuming power or exponential models indicates that in situ hydrostatic pressure and/or food/chemical energy availability are responsible for variation in holothurian metabolic rates. Consequently, these results have implications for modelling deep-sea energetics and processes.

Demographic indicators of change in a deposit-feeding abyssal holothurian community (Station M, 4000 m)

Holothurians are among the most abundant benthic megafauna at abyssal depths, and important consumers and bioturbators of organic carbon on the sea floor. Significant fluctuations in abyssal holothurian density are often attributed to species-specific responses to variable particulate organic carbon flux (food supply) stemming from surface ocean events. We report changes in densities of 19 holothurian species at the abyssal monitoring site Station M in the northeast Pacific, recorded during 11 remotely operated vehicle surveys between Dec 2006 and Oct 2014. Body size demographics are presented for Abyssocucumis abyssorum, Synallactidae sp. 1, Paelopatides confundens, Elpidia sp. A, Peniagone gracilis, Peniagone papillata, Peniagone vitrea, Peniagone sp. A, Peniagone sp. 1, and Scotoplanes globosa. Densities were lower and species evenness was higher from 2006–2009 compared to 2011–2014. Food supply of freshly-settled phytodetritus was exceptionally high during this latter period. Based on relationships between median body length and density, numerous immigration and juvenile recruitment events of multiple species appeared to take place between 2011 and 2014. These patterns were dominated by elpidiids (Holothuroidea: Elasipodida: Elpidiidae), which consistently increased in density during a period of high food availability, while other groups showed inconsistent responses. We considered minimum body length to be a proxy for size at juvenile recruitment. Patterns in density clustered by this measure, which was a stronger predictor of maximum density than median and mean body length.

Phytopigments as biomarkers of selectivity in abyssal holothurians; interspecific differences in response to a changing food supply

Holothurians dominate the abyssal megabenthos. They are key consumers and bioturbators of surficial sediment. Compounds essential for holothurian reproduction, such as carotenoids, are in short supply in the deep ocean. Holothurians cannot synthesise carotenoids de novo; the compounds are supplied with the flux of phytodetritus. Therefore, the supply of these compounds may play an important role in regulating processes on the seafloor. This study examines the link between the diet of abyssal holothurians and their ovarian carotenoid biochemistry. Phytodetritus, surficial sediment, holothurian gut content and ovaries were sampled in June 2004 and in July 2005 at the Porcupine Abyssal Plain (PAP), NE Atlantic. Gut content chlorophyll a concentration showed that Amperima rosea, Peniagone diaphana and Oneirophanta mutabilis fed selectively on fresh organic matter, although when this was scarce, O. mutabilis was outcompeted and fed on more refractory material. All three species display consistent ovarian carotenoid profiles and have relatively high carotenoid concentrations in their ovaries. Psychropotes longicauda, Paroriza prouhoi, Pseudostichopus aemulatus, P. villosus and Molpadia blakei fed less selectively and exhibited low ovarian carotenoid concentrations with inconsistent profiles. The results suggest that abyssal holothurian ovarian biochemistry is a complex function of OM supply, holothurian feeding guild and reproductive adaptation. Changes in upper ocean biogeochemistry, altering the composition of organic matter reaching the deep-sea floor, may favour certain holothurian species, as suggested by the interspecific differences in holothurian ovarian biochemistry. This may lead to large community changes as seen at the PAP, which can alter the reworking rates of sediment, probably affecting carbon burial. The study also demonstrated that using the presence of biomarkers in gut contents to infer feeding selectivity should be used with caution. Only biomarkers in gut contents that are not present in the tissues of the holothurians (e.g., chlorophyll a) should be used to determine their feeding selectivity.

A new genus and species of Brychiopontiidae Humes, 1974 (Crustacea: Copepoda: Siphonostomatoida) associated with an abyssal holothurian in the Northeast Pacific nodule province *

A new genus and species of Brychiopontiidae Humes, 1974 (Crustacea: Copepoda: Siphonostomatoida) associated with an abyssal holothurian in the Northeast Pacific nodule province *

A new genus and species of Brychiopontiidae Humes, 1974 (Crustacea: Copepoda:Siphonostomatoida) associated with an abyssal holothurian in the NortheastPacific nodule province

A new genus and species Neobrychiopontius galeronae gen. nov. sp. nov. is described based on female specimens from the Pacific nodule province associated with the abyssal holothurian Oneirophanta cfr. setigera (Ludwig, 1894) (Elasipodida, Deimatidae). The holothurian and copepods were collected at a depth of 4978 m during the cruise “Nodinaut” (Ifremer, 17 May – 28 June 2004) on RV Atalante using a spade corer operated from the submersible Nautile. The new genus has retained a greater number of plesiomorphic characters, when compared to its closest relative the monotypic genus Brychiopontius Humes, 1974 from the abyssal zone of the North Atlantic: proximal 3 segments of antennule articulates (fused in Brychiopontius), well developed mandibular palp and inner lobe of maxilla (both absent in Brychiopontius). On the other hand the new genus has only 2 outer spines on the third exopodal segment of leg 1 (instead of 3 in Brychiopontius). Two plesiomorphic characters hitherto unknown for the order Siphonostomatoida are present in the new genus viz. the inner lobe of the first segment of the maxilla is armed with 2 setae and the first segment of the mandibular palp is armed with 1 seta. Neobrychiopontius galeronae gen. et sp. nov. is the second species of Siphonostomatoida found in association with abyssal holothurians (both belonging to the genus Oneirophanta) and represents the first record of the family Brychiopontiidae in the Pacific Ocean.

Lipid, sterols and fatty acid composition of abyssal holothurians and ophiuroids from the North-East Pacific Ocean: Food web implications

The lipid, fatty acid (FA), and sterol composition of two ophiuroids and four holothurians from the abyssal eastern North Pacific were analysed to assess their feeding habits and to ascertain their composition for use in a larger study to examine food web dynamics and trophic ecology. Holothurians were rich in phytosterols and algal derived FA such as docosahexaenoic acid and eicosapentaenoic suggesting tight trophic coupling to phytodetritus. Large proportions of stanols were found, probably a result of enteric bacteria but they may come from sterol metabolism in the holothurians themselves. Oneirophanta mutabilis was distinct with much higher levels of stanols and bacterially derived FA suggesting specific selection of bacteria rich detrital particles or the activity of enteric and integumental bacteria. The ophiuroids sterol and FA compositions differed greatly from the holothurians and reflected consumption of animal material in addition to phytodetritus. Large proportions of energy storage lipids suggested a sporadic food supply. Several unusual fatty acids were found in these abyssal echinoderms. Tetracosahexaenoic acid, 24:6ω3, in ophiuroids and 23:1 in holothurians may be good biomarkers for food web studies. We report the first occurrence of αOH 24:1 in holothurians with none detected in ophiuroids. Its function is presently unknown.

Reproductive biology of the abyssal holothurian Amperima rosea: an opportunistic response to variable flux of surface derived organic matter?

A radical change in the abundance of invertebrate megafauna has occurred over a vast area of the Porcupine Abyssal Plain, north-east Atlantic, in recent years. In particular, the holothurian Amperima rosea has increased in abundance by three orders of magnitude. The sudden increase in abundance of A. rosea appears to be the result of environmental forcing rather than localized stochastic population variations. Amperima rosea produces small eggs ([les ]200 μm) indicating (1) planktotrophic larval development or (2) lecithotrophic larval development with an abbreviated larval stage. It also reaches maturity at a very small size. The reproductive biology of A. rosea indicates that it can increase rapidly in population size and can colonize large areas quickly. It has high fecundity, as predicted by gonad indices and observed in histological studies. Fecundity was greater in winter than in summer months, but there was no clear evidence of seasonal or episodic reproductive events. All males, irrespective of sample season or year, were mature with spermatozoa. Most oocytes were of an intermediate size (70 to 120 μm), either at the late previtellogenic (70–90 μm) or early vitellogenic (100–120 μm) stage of development. It is postulated that development of full vitellogenesis, leading to episodic spawning, might be dependent on certain environmental stimuli. The most likely stimulus is food supply. Amperima rosea has been shown to feed preferentially on phytodetritus and to have a requirement for certain sterols in its diet. Qualitative changes in the flux of organic matter to the sea-floor may control vitellogenesis and fecundity, and hence have an effect on the population dynamics of the species.

A preliminary investigation of the lipids of abyssal holothurians from the north-east Atlantic Ocean

The dominant lipids of seven species of abyssal holothurians (Oneirophanta mutabilis, Pseudostichopus villosus, Psychropotes longicauda, Deima validium, Parariza prouhoi, Amperima rosea and Molpadia blakei) have been examined in detail. Fatty acid compositions are qualitatively similar to those of shallow-water holothurians, but relatively higher amounts of unsaturated compounds in the deep sea animals are ascribed to an adaptation of the latter to maintain membrane fluidity at high pressure and low temperature. The sterol distributions of abyssal holothurians are complex, with mixtures of C26–C30 sterols being present in all of the animals. These are most likely to be dietary in origin; the holothurians substitute Δ5 with Δ7 unsaturation, via Δ5,7 or Δ0 intermediates. 14α-methylcholest-9(11)-enol, which is a common product of de novo biosynthesis in shallow-water holothurians is absent in all of the deep-water species. Furthermore, cholest-7-enol, the dominant product of de novo biosynthesis in shallow water animals, is a relatively minor component in all of the species, except A. rosea. This holothurian is also the only one that appears to assimilate 4α-methylsterols directly and contains high amounts of steryl sulphates. There are significant interspecies differences in the free sterol distributions which may reflect their different feeding strategies or niches.

An association between Exspina typica Lang (Tanaidacea) and deep-sea holothurians

First reports of the association between Exspina typica and three species of abyssal holothurian are presented. These records suggest that the association is a real one, and not an artefact of sampling, but throw no light on the nature of the association. The geographic and bathymetric distributions of E. typica are summarized, and the species is shown to be a widely distributed cold water stenotherm.

Relations between amino acid composition of sinking particles, gut content of abyssal holothurians and surrounding sediment : Alberic, P. and A. Khripounoff, 1984. Mar. Chem., 14(4):379–394. (In French, English abstracts.) Lab. de Geol. Appliq., ERA 601 du CNRS, Univ. d'Orleans, 45046 Orleans Cedex, France

Relations between amino acid composition of sinking particles, gut content of abyssal holothurians and surrounding sediment : Alberic, P. and A. Khripounoff, 1984. Mar. Chem., 14(4):379–394. (In French, English abstracts.) Lab. de Geol. Appliq., ERA 601 du CNRS, Univ. d'Orleans, 45046 Orleans Cedex, France

Barophilic Bacteria Associated with Digestive Tracts of Abyssal Holothurians

Abyssal holothurians and sediment samples were collected at depths of 4,430 to 4,850 m in the Demerara abyssal plain. Bacterial concentrations in progressive sections of the holothurian digestive tract, as well as in surrounding surface sediments, were determined by epifluorescence microscopy. Total bacterial counts in sediments recently ingested by the animals were 1.5- to 3-fold higher than in surrounding sediments at the deepest station. Lowest counts were observed consistently in the foregut, where the digestive processes of the holothurian are believed to occur. In most animals, counts increased 3- to 10-fold in the hindgut. Microbial activity at 3 degrees C and in situ and atmospheric pressure were determined for gut and sediment samples by measuring the utilization of [C]glutamic acid, the doubling time of the mixed-population of culturable bacteria, and the percentage of the total bacterial count responsive to yeast extract in the presence of nalidixic acid, using epifluorescence microscopy. A barophilic microbial population, showing elevated activity under deep-sea pressure, was detected by all three methods in sediments removed from the hindgut. Transmission electron micrographs revealed intact bacteria directly associated with the intestinal lining only in the hindgut. The bacteria are believed to be carried as an actively metabolizing, commensal gut flora that transforms organic matter present in abyssal sediments ingested by the holothurian. Using data obtained in this study, it was calculated that sediment containing organic matter altered by microbial activity cleared the holothurian gut every 16 h, suggesting that abyssal holothurians and their associated gut flora are important participants in nutrient cycles of the abyssal benthic ocean.

New cyclopoid copepods associated with an abyssal holothurian in the eastern North Atlantic

New cyclopoid copepods associated with an abyssal holothurian in the eastern North Atlantic