Morphological adaptations to chronic hypoxia in deep-sea decapod crustaceans from hydrothermal vents and cold seeps

Animals inhabiting hydrothermal vents and cold seeps face conditions that are challenging for survival. In particular, these two habitats are characterized by chronic hypoxia, sometimes reaching complete anoxia. The characteristics of the scaphognathite and gills were studied in four species of shrimp and three species of crabs from hydrothermal vents and cold seeps, in order to highlight potential adaptations that could enhance oxygen acquisition in comparison with shallow-water relatives. All the vent and seep species studied here exhibit significantly larger scaphognathites, likely allowing more water to flow over their gills per stroke of this appendage. This is probably more energetically efficient that prolonged hyperventilation. In contrast to annelids, vent and seep decapods usually do not possess enlarged gills, a phenomenon likely due to the physical limitations imposed by the size of the gill chamber. In the vent shrimp Rimicaris exoculata and the vent crab Bythograea thermydron, however, there is a significantly higher specific gill surface area linked to a higher number of lamellae per gram of gill. Again in contrast to annelids, the diffusion distance through the gills is not strikingly different between the vent shrimp Alvinocaris komaii and the shallow-water species Palaemon spp. This may indicate that the epithelium and cuticle of the decapod gills are already optimized for oxygen uptake and that reducing the thickness of these compartments is not physically possible without affecting the physical integrity of the gills.     

Metabolism of shallow and deep-sea benthic crustaceans and echinoderms in Hawaii

Little is known about the metabolism of deep-living, benthic invertebrates, despite its importance in estimating energy flow through individuals and populations. To evaluate the effects of depth and broad taxonomic group/locomotory mode, we measured the respiration rates of 25 species of benthic decapod crustaceans and 18 species of echinoderms from the littoral zone to the deep slope of Hawaii. Specimens were collected by hand, trap, or submersible and maintained in the laboratory at temperatures close to ambient temperatures recorded at the time of collection. After acclimatization to laboratory conditions, oxygen consumption was measured for each individual in closed chambers. Overall, crustaceans had higher metabolic rates than echinoderms, and within the crustaceans, caridean shrimps had higher rates than crabs and lobsters. These differences are probably related to locomotory mode and general levels of activity. At in situ environmental temperatures, metabolic rates of deeper-living invertebrates are much lower than those of shallower living species, but this decline is explained by changes in temperature. When the data were compared with similar data sets collected off California and in the Mediterranean, Hawaiian crabs, lobsters, and echinoderms had lower metabolic rates than similar species in the other regions after adjustments for temperature were made. Some of these differences could be methodological. Regional food web models should use broad taxonomic groupings and region-specific data when possible.     

Comparative study of behavioral-sensitivity thresholds to near-UV and blue-green light in deep-sea crustaceans

The behavioral sensitivities of five species of deep-sea crustaceans (order Decapoda: Acanthephyra curtirostris, A. smithi, Notostomus gibbosus, Janicella spinacauda and Oplophorus gracilirostris) to near-UV and blue-green light were studied during a research cruise off the coast of Hawaii in 1993. Two of the five species have electrophysiologically-measured spectral sensitivity peaks at 400 and 500 nm, while the remaining three species have a single sensitivity peak at 490 to 500 nm. In the current study, behavioral mean threshold sensitivities (defined as the lowest irradiance change to which the shrimp would give a behavioral response) were determined for tethered specimens of each species at two wavelengths, 400 and 500 nm. The mean behavioral threshold sensitivities of the two species with putative dual visual-pigment systems were approximately the same to near-UV and blue-green light, while the other three species were significantly less sensitive to near-UV vs blue-green light. Results from these experiments indicate that (1) behavioral information obtained from tethered shrimp accurately reflects their spectral sensitivity, and (2) the sensitivity of the putative dichromats to near-UV light is sufficiently low to detect calculated levels of near-UV light remaining in the down-welling field at their daytime depth of 600 m. Possible functions of this high sensitivity to short wavelength light are discussed.     

Temporal variability of deep-sea zooplankton in the Arabian Sea

Mesozooplankton samples from two stations in the Arabian Sea (WAST, 4,050 m, 16°15′N, 60°20′E; CAST, 3,950 m, 14°30′N, 64°30′E) were collected from the surface down to 20 m above bottom during three monsoon periods: the autumn intermonsoon in October 1995, the spring intermonsoon in April 1997, and the NE monsoon in February 1998. The main goal of this study is to enhance our knowledge on the effect of spatial and temporal differences in primary production and particle flux rates on the abundance and distribution of mesozooplankton, with special attention to the deep sea. Literature data indicate episodically high rates of primary production and particle flux in the region during the SW monsoon and the autumn intermonsoon. Set in this context, the zooplankton showed an in-phase coupling in biomass and abundance with the primary production in the surface 150 m. In the mesopelagic realm (150–1,050 m), the seasonal coupling was less clear. In the bathypelagic zone, below 1,050 m, there was no evidence of in-phase coupling, though temporal differences in the distribution of zooplankton abundance and biomass with depth between seasons could be shown by an analysis of covariance and an a posteriori test. The results suggest that the bathypelagic community responds to increased particle flux rates, but with longer time gaps than in the epipelagic zone. This is probably due to longer development and response times of zooplankton in the cold, deep-water environment, independent of possible lateral advection processes.     

Temporal resolution in the eyes of marine decapods from coastal and deep-sea habitats

 Temporal responses of eyes from four decapod species taken from sublittoral (Pandalus montagui Leach), coastal [Nephrops norvegicus (L.)] and deep-sea [Paromola cuvieri (Risso) and Chaceon (=Geryon) affinis A. Milne Edwards and Bouvier] habitats were examined. The electroretinogram responses to a range of sinusoidal intensity modulations between 0.5 and 40 Hz were recorded. Recordings were made from individuals adapted successively to two background light intensities. The sublittoral and coastal species showed faster responses when adapted to the higher light level and they also responded best to intermediate frequencies. When adapted to the lower light level, all species responded most strongly to low-frequency stimuli. Physiological and ecological reasons for the differences in responses are suggested. Received: 2 July 1999 / Accepted: 26 October 1999     

Temporal patterns in diversity and species composition of deep-sea benthic copepods in bathyal Sagami Bay,central Japan

Little is known about temporal changes in the diversity and species composition of deep-sea metazoan meiofauna and their relationships with changes in the food supply. Those changes were studied for benthic copepod assemblages based on 2-year time-series data at a bathyal site in Sagami Bay (1430 m depth), central Japan, where annual fluctuation in the abundance of benthic foraminiferans was previously observed. Species diversity of benthic copepods at the site was as high as, or slightly higher than, that observed at other deep-sea sites, but did not fluctuate temporally through the study period. Multivariate analyses did not reveal any clear seasonal or directional change occurring over the longer term in their species composition, although there was some consistent pattern. These results indicate a lack of, or only weak, seasonality in the diversity and species structure of the deep-sea benthic copepod assemblages, even though the fresh organic food supply fluctuates seasonally. They also suggest that there are differences between copepods and foraminiferans in the response to changes in environmental factors, and that spatial differences in the composition of copepod communities are greater than temporal ones at this deep-sea site.Communicated by T. Ikeda, Hakodate     

Fluoride in Antarctic marine crustaceans

The concentration of fluoride in the body parts of a range of Antarctic crustaceans from a variety of habits was examined with the aim of determining whether fluoride concentration is related to lifestyle or phylogenetic grouping. Euphausiids had the highest overall fluoride concentrations of a range of Antarctic marine crustaceans examined; levels of up to 5477 μg g⁻¹ were found in the exoskeleton of Euphausia crystallorophias. Copepods had the lowest fluoride levels (0.87 μg g⁻¹ whole-body); some amphipods and mysids also exhibited relatively high fluoride levels. There was no apparent relationship between the lifestyle of the crustaceans and their fluoride level; benthic and pelagic species exhibited both high and low fluoride levels. Fluoride was concentrated in the exoskeleton, but not evenly distributed through it; the exoskeleton of the head, carapace and abdomen contained the highest concentrations of fluoride, followed by the feeding basket and pleopods, and the eyes. The mouthparts of E.␣superba contained almost 13 000 μg F g⁻¹ dry wt. Antarctic krill tail muscle had low levels of fluoride. After long-term (1 to 5 yr) storage in formalin, fluoride was almost completely lost from whole euphausiids. Received: 1 April 1998 / Accepted: 29 July 1998     

Biosynthesis of wax esters in oceanic crustaceans

Slices from the hepatopancreas of various oceanic curstaceans incorporated radioactivity into wax esters from ¹⁴C glucose and ¹⁴C aspartic acid to a lesser extent and from ¹⁴C palmitic acid to a much greater extent. Radioactivity was incorporated from ¹⁴C palmitic acid into both fatty acid and fatty alcohol moieties of wax esters, the percentage of total radioactivity present in alcohol moieties being greater in deep-living than in shallow-living species. Cell-free preparations from the hepatopancreas but not from muscle, supplemented with ATP and reduced pyridine nucleotides, incorporated radioactivity from 1-¹⁴C palmitoyl Coenzyme A into both fatty alcohol and fatty acid moieties of wax esters. Incorporation into fatty alcohol was NADPH- rather than NADH-specific. Preparations from deep-living species had a greater percentage of total radioactivity in the fatty alcohol moieties of wax esters than preparations from shallow-living species. We conclude that the level of wax esters in a given species is correlated with the rate at which the species biosynthesises these lipids de novo; deep-living species have higher rates of wax ester biosynthesis and higher levels of wax esters than shallow-living species. The results support the thesis that wax esters in oceanic crustaceans are derived largely from the animals' internal biosynthetic activities, presumably in response to particular biochemical and/or physiological requirements, rather than from their diets.     

Carbohydrate metabolism of two crustaceans during starvation

In Emerita asiatica and Ligia exotica, starvation for 1 week steadily depleted the free sugar values, indicating their involvement in nutritive physiology. Protein-bound blood sugars showed no change during starvation, indicating their non-involvement in general carbohydrate metabolism; it is suggested that they may be involved in the moulting physiology related to the synthesis of structural components such as chitin. The extent of glycogen storage is found to be greater in the anomuran E. asiatica than in the isopod L. exotica. In the latter, the fall in free sugar values during starvation is greater, due to meagre storage of glycogen in the hepatopancreas. these features are related to habitat and availability of food in the environment.     

Carbonic anhydrase in deep-sea chemoautotrophic symbioses

Carbonic anhydrase (CA) facilitates the rapid interconversion of carbon dioxide and bicarbonate. It is ubiquitous among organisms, and participates in numerous cellular processes. In several photoautotrophic marine organisms, CA facilitates uptake of inorganic carbon by catalyzing the reversible dehydration of bicarbonate to carbon dioxide, which diffuses more rapidly across cell membranes. In algal/invertebrate symbioses, this mechanism is correlated with significantly elevated CA activity in tissues where zooxanthellae are housed. Here, we determine whether elevated CA activity is also characteristic of tissues involved in inorganic carbon uptake by chemosynthetic invertebrates. Measurements of CA activity in several chemosynthetic clam and vestimentiferan species indicate that CA facilitates inorganic carbon uptake, with high activities present in clam gill tissue, and vestimentiferan plume and trophosome tissues. However levels of CA activity among species varied widely, from very low in mytilids to extraordinarily high in some vesicomyids and vestimentiferans. High CA activity is generally correlated with other adaptations for control of internal chemical environments where symbionts are housed, such as the presence of serum-borne sulfide-binding moieties. These findings suggest that a CA-based mechanism of carbon uptake may be one of a suite of adaptations to provide symbionts with essential metabolites.     

Trophic structure of deep-sea macrobenthos

The effect of the trophic factor on large-scale distributional patterns of deep-sea macrobenthos inhabiting the floor of the World Ocean has been studied. Two hundred and twenty-eight bottom trawl samples collected by Soviet research vessels in the Pacific and Indian Oceans at depths ranging from 3000 to 6000 m were analyzed. For each sample, the weight of animals with a similar mode of feeding was determined to find the weight ratio of representatives of three main trophic groups, i.e., deposit-feeders, suspension-feeders and carnivores. These data, indicating predominance of alternate groups as well as data on their geographic distribution, were related to feeding conditions which depend on: (1) rates of sedimentation, (2) nature of sediments, (3) content of organic carbon, (4) degree of transformation of organic matter on and within sediments, and, when available, (5) data on redox potential, biochemical oxygen consumption, and state of heterotrophic microflora in the sediments. In dealing with the feeding conditions of deep-sea macrobenthos in the Atlantic Ocean, biological characteristics were deduced from literature data on the composition of sediments, their redox potential and organic carbon content. As a result of this research, eutrophic and oligotrophic regions on the floor of the World Ocean have been distinguished and their boundaries defined. Eutrophic regions lie within areas with high biological productivity of surface-water layers, and cover the peripheral and equatorial parts of the oceans; they are characterized by quantities of labile (digestible) organic matter within sediments which are sufficient for deposit-feeders to predominate in eutrophic regions everywhere, except on considerable bottom elevations. Oligotrophic regions are confined to open areas of the oceans lying beyond the equatorial belt; they are characterized by very low rates of sedimentation and, consequently, by scarce quantities of deposited organic matter. Here, suspension-feeders predominate, although their population density is very low.     

Life-history adaptations to arboreality in snakes

If selective forces on locomotor ability and reproductive biology differ among habitats, we expect to see relationships between habitat, morphology, and life-history traits. Comparative (phylogenetically based) analysis of data from 12 pythonid and 12 boid snake species reveals multiple evolutionary shifts in habitat use, notably in the evolution of arboreal habits. Compared to terrestrial and aquatic taxa of the same overall body size, arboreal species have narrower and more laterally compressed bodies and relatively longer tails. Offspring sizes are not affected by arboreality, but presumably reflecting space constraints within their narrow bodies, arboreal species (1) produce smaller clutch sizes relative to maternal body length and (2) have left and right ovaries that overlap little if at all along the length of the body (i.e., the right ovary is positioned anterior to the left ovary) whereas in terrestrial snakes the two ovaries overlap along much of their length. This modification of ovarian morphology in arboreal snakes presumably reduces the degree of bodily distension during vitellogenesis and pregnancy, thus enhancing climbing ability and camouflage among the branches.     

Correlation between photosensitivity and downwelling irradiance in mesopelagic crustaceans

The current study determined behavioral and electrophysiological photosensitivities for three species of mesopelagic crustaceans: Pasiphaea multidentata Esmark, 1866 (Decapoda: Pasiphaeidae), Sergestes arcticus Kröyer, 1855 (Decapoda: Sergestidae), and Meganyctiphanes norvegica M. Sars, 1857 (Euphausiacea: Euphausiidae). In addition, in situ quantifications of the species vertical distributions in relation to downwelling irradiances were also determined in two locations in the northwest Atlantic Ocean, Wilkinson Basin (WB) and Oceanographer Canyon (OC). Data are from six 2-week cruises between June and September from 1995 to 2001. P. multidentata and M. norvegica were the most abundant large crustaceans in WB, and S. arcticus and M. norvegica were the most abundant large crustaceans in OC. The behavioral light sensitivity thresholds of P. multidentata and M. norvegica from WB were both 10⁷ photons cm^–2 s^–1 and those of S. arcticus and M. norvegica from OC were both 10⁸ photons cm^–2 s^–1. Electrophysiologically, P. multidentata was significantly more sensitive than M. norvegica from either location, S. arcticus was significantly more sensitive than M. norvegica from OC, and M. norvegica from WB was significantly more sensitive than M. norvegica from OC. A correlation was found between electrophysiologically measured photosensitivity and downwelling irradiance, with the most sensitive species, P. multidentata and S. arcticus, associated with the lowest irradiance at daytime depths. The photosensitivities of M. norvegica collected from the clearer waters of OC were significantly lower than those of individuals collected from the more turbid WB waters. These results indicate that downwelling irradiance has a significant impact on interspecies and intraspecies vertical distribution patterns in the mesopelagic realm.Communicated by J.P. Grassle, New Brunswick     

Coelenterazine distribution and luciferase characteristics in oceanic decapod crustaceans

Coelenterazine biosynthesis has recently been demonstrated in the developing eggs of the decapod Systellaspis debilis. The cellular source of coelenterazine and the potential for biosynthesis in adult decapods, however, have not been fully investigated. We have conducted a systematic study of coelenterazine content in >230 individual decapods representing 19 species of Oplophoridae and 22 species from other families. We show for the first time that coelenterazine is responsible for both secretory and photophore luminescence in the same decapod. Tissues associated with secretory luminescence (hepatopancreas and stomach) in the Oplophoridae contained almost 3 orders of magnitude more coelenterazine (mean value=2154 pmol per specimen) than cuticular photophores (mean value=8 pmol per specimen). Coelenterazine content increases by 2 to 4 orders of magnitude during the development of three species of Oplophoridae. Species of Oplophoridae contain an order of magnitude more coelenterazine than those of other families (mean value=154 pmol per specimen). Coelenterazine was also detected in 11 apparently nonluminous decapod species (mean value=200 pmol per specimen). S. debilis luciferase characterisation enabled a luciferase assay to be developed to facilitate studies of the environmental control of bioluminescence. We hypothesise that the coelenterazine requirement in secretory bioluminescence exceeds that which could be assimilated from the food-chain. The significant increase of coelenterazine during the life cycle of secretory decapods supports this hypothesis. Putative evidence for environmental control of coelenterazine luminescence is also reported.     

Composite forces shape population dynamics of copepod crustaceans

Understanding the processes that control species abundance and distribution is a major challenge in ecology, yet for a large number of potentially important organisms, we know little about the biotic and abiotic factors that influence population size. One group of aquatic organisms that defies traditional demographic analyses is the Crustacea, particularly those with complex life cycles. We used likelihood techniques and information theoretics to evaluate a suite of models representing alternative hypotheses on factors controlling the abundance of two copepod crustaceans in a small, tropical floodplain lake. Quantitative zooplankton samples were collected at three stations in a Venezuelan floodplain lake from June through December 1984; the average sampling interval was two days. We constructed a series of models with stage structure that incorporated six biotic and abiotic covariates in various combinations to account for temporal changes in abundance of these target species and in their population growth rates. Our analysis produced several novel insights into copepod population dynamics. We found that multiple forces affected the abundance of particular stages, that these factors differed between species as well as among stages within each species, and that biotic processes had the largest effects on copepod population dynamics. Density dependence had a large effect on the survival of Oithona amazonica copepodites and on population growth rate of Diaptomus negrensis.     

Leaf choice by crustaceans in a mangrove forest in Queensland

The feeding behaviour of leaf eating crustaceans feeding on leaves shed by Avicennia marina, Bruguiera gymnorhiza and Rhizophora stylosa in the mangrove forest at Myora Springs, Queensland, Australia was studied between 1980 and 1984. Individual Sesarma erythrodactyla (carapace >9 mm long), one of the most abundant species of crabs in the forest, processed approximately half a leaf from any of the three species of mangroves in 24 h under laboratory conditions. of the amount of leaf material processed, 20% was lost from the mandibles due to sloppy feeding, 68% was egested as faeces and 12% converted into crab biomass. Crabs processed more leaf material at 30°C than at 20°C. S. erythrodactyla preferred leaves of A. marina to those of the other two species, probably because leaves of A. marina have a lower tannin and a higher nitrogen content. Of the other two species, B. gymnorhiza was preferred to R. stylosa. Among leaves of R. stylosa, S. erythrodactyla exerts a strong preference for aged rather than freshly fallen, and for thick rather than thin leaves. The mesofauna (carapace length <9.0 mm) which processed dead mangrove leaves comprised juveniles of S. erythrodactyla, the crab Ilyograpsus paludicola, the isopod Exosphaeroma alata and the amphipods Orchestia sp. and Melita sp. These species processed between 0.2 and 24.7 mg dry wt of a leaf per individual over a period of 4 d. Of this, 72 to 85% was egested as faeces. The significance of leaf eating crabs to nutrient cycling in mangrove forests is discussed. I conclude that leaf processing by crustaceans shortens the time span between leaf fall and consumption of leaf material by organisms. This may have the effect of conserving leaf biomass inside the mangrove forest.     

Reproductive biology in two species of deep-sea squids

Deep-sea squids, Moroteuthis ingens and Gonatus antarcticus, were collected in the slope waters off the Falkland Islands and their reproductive systems preserved and investigated onshore. Changes in oocyte length-frequencies at maturation and spawning, and their fecundity were studied. These squids, as well as many other species, are characterised by a synchronous oocyte growth and ovulation. Oviducts are not used for ripe egg accumulation and consequently the universal scale of Lipinski (1979) cannot be applied to assign female maturity. M. ingens spawns near the bottom; its fecundity is 168–297 thousand eggs. Maximum egg size is 1.8–2.7 mm. G. antarcticus spawns midwater; its fecundity is 10–25 thousand eggs. Egg size is 3.2–3.3 mm. In M. ingens spawning takes place in the austral autumn and winter, in G. antarcticus—in austral winter. Our data and the literature data show that the so-called “synchronous ovulation” probably occurs in all deepwater squids. This pattern is very rare among fish, but is quite common among benthic octopods that brood their egg masses.     

Vitellogenesis in the deep-sea shark Centroscymnus coelolepis

At present, information on the reproductive physiology of Centroscymnus coelolepis, which is one of most important and widespread deep-sea shark species, is completely lacking. In this study, we investigated vitellogenesis, a key step in the reproduction biology of fishes. Specimens of C. coelolepis were collected at 2850 m depth in the Western Mediterranean Sea. The size of the collected sharks (range: 35.5-65.0 cm TL) was much lower than those typically reported for the Atlantic and Pacific Oceans. The marked distinctiveness of Mediterranean and Atlantic/Pacific populations was reflected by the achievement of sexual maturity at a smaller size in Mediterranean specimens. The examination of cytoplasmatic components of oocytes indicated that vitellogenin uptake in the ovary started when oocytes reached 14 mm in diameter. Only reproductive females displayed a significant relationship between plasmatic vitellogenin and gonadal development, suggesting that vitellogenesis in C. coelolepis is a discontinuous process. Oestradiol levels were tightly coupled with gonadal development, underlining the importance of this hormone in controlling vitellogenesis. All these findings suggest that vitellogenesis in this yolk-sac viviparous shark might occur with similar mechanisms of oviparous vertebrates.     

Vitellogenesis in the deep-sea shark Centroscymnus coelolepis

At present, information on the reproductive physiology of Centroscymnus coelolepis, which is one of most important and widespread deep-sea shark species, is completely lacking. In this study, we investigated vitellogenesis, a key step in the reproduction biology of fishes. Specimens of C. coelolepis were collected at 2850 m depth in the Western Mediterranean Sea. The size of the collected sharks (range: 35.5–65.0 cm TL) was much lower than those typically reported for the Atlantic and Pacific Oceans. The marked distinctiveness of Mediterranean and Atlantic/Pacific populations was reflected by the achievement of sexual maturity at a smaller size in Mediterranean specimens. The examination of cytoplasmatic components of oocytes indicated that vitellogenin uptake in the ovary started when oocytes reached 14 mm in diameter. Only reproductive females displayed a significant relationship between plasmatic vitellogenin and gonadal development, suggesting that vitellogenesis in C. coelolepis is a discontinuous process. Oestradiol levels were tightly coupled with gonadal development, underlining the importance of this hormone in controlling vitellogenesis. All these findings suggest that vitellogenesis in this yolk-sac viviparous shark might occur with similar mechanisms of oviparous vertebrates.     

Studies on the lipid metabolism of some oceanic crustaceans

Mid-water, oceanic crustaceans were either fed food labelled with (¹⁴C) palmitic acid under controlled conditions, or injected directly with (¹⁴C) palmitic acid. Lipid classes and their constituent fatty acids and fatty alcohols were subsequently separated and assayed for radioactivity. Significant levels of radioactivity were present in the 16:0¹ alcohols and 18:1 acids of wax esters, and in the 16:0/16:1, 18:0/18:1, 20:5 and 22:6 acids of both triglycerides and phospholipids. It was concluded that these crustaceans were capable of biosynthesis of wax esters and higher polyunsaturated fatty acids.