Evolutionary relationships among deep-sea mytilids (Bivalvia: Mytilidae) from hydrothermal vents and cold-water methane/sulfide seeps

A protein electrophoretic survey of mytilids inhabiting deep-sea hydrothermal vents and cold-water methane/sulfide seeps revealed electromorph patterns diagnostic of 10 distinct species. From hydrothermal vents located at sites on the Galápagos Rift, the Mid-Atlantic Ridge, and the Mariana Back Arc Basin, we detected four species of mytilids. Six additional species were detected from three cold-water seep sides in the Gulf of Mexico. The patchy distribution and temporal stability of seeps may provide a greater opportunity for mytilid diversification and persistence than vent sites Nei's genetic distances (D) between species were relatively large (range: 0.528 to ) both within and among habitat types. This pronounced degree of genetic differentiation suggests a relatively ancient common ancestor for the group. Phylogenetic trees were generated using distance Wagner and parsimony analyses of allozyme and morphological characters. The tree topologies obtained from both methods support: (1) the hypothesis that a seep ancestor gave rise to the deep-sea hydrothermal vent mytilids, (2) a historical progression from shallow-water to deep-water habitats, and (3) a co-evolutionary progression from external to internal localization of bacterial symbionts. Whether the seep mytilid taxa constitute paraphyletic or polyphyletic groups remains unresolved. Our phylogenetic hypotheses also provide a benchmark for the phylogeny of mytilid bacterial symbionts.     

Influence of habitat on the reproductive biology of the deep-sea hydrothermal vent limpet <Emphasis Type="Italic">Lepetodrilus fucensis</Emphasis> (Vetigastropoda: Mollusca) from the Northeast Pacific

Habitat selection by the hydrothermal vent limpet, Lepetodrilus fucensis, in Northeast Pacific hydrothermal vent ecosystems, may influence its reproductive output, as it occupies habitats with varying physico-chemical conditions that reflect the availability of nutritional resources. Histological techniques were used to determine size at first reproduction, gametogenesis, reproductive output, and fecundity in relation to shell length (SL), through examination of the gonads of male and female L. fucensis, collected from five different hydrothermal vent habitat types with different temperature anomalies and hydrothermal fluid flow vigour: vigorous (VIG), diffuse (DIF), tubeworm bushes (TWB), peripheral (PER), and senescent areas (SEN). Both male and female L. fucensis exhibited early maturity, with the first reproductive event occurring at 3.8 and 3.9 mm shell length, respectively. All stages of gamete development were present in the gonads of males and females, suggesting continuous gametogenesis and asynchronous reproduction in this species. Gametogenic maturity of limpets did not vary among actively venting habitats (VIG, DIF, TWB, and PER), but was significantly lower in males and females from SEN habitats. Mean oocyte diameter was largest in females from VIG habitats, and smallest in females from SEN habitats, than in those from the other habitats (DIF, TWB, and PER). Females from actively venting habitats also had greater actual fecundity than those from senescent habitats. While the gametogenic pattern of L. fucensis appears phylogenetically constrained, selection of actively venting habitats by L. fucensis maximizes its reproductive output. The multiple feeding strategies of L. fucensis may allow for a constant supply of energy to be allocated to reproduction in any habitat except senescent vents. Early maturity, high fecundity, and continuous production of gametes suggest a reproductive strategy characteristic of an opportunistic species, and may be contributing to the extremely abundant populations of L. fucensis observed in the Northeast Pacific vent ecosystem.     

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.     

Population structure of two deep-sea hydrothermal vent gastropods from the Juan de Fuca Ridge, NE Pacific

The gastropods Lepetodrilus fucensis and Depressigyra globulus are abundant faunal components of animal communities at deep-sea hydrothermal vents along the Juan de Fuca Ridge in the NE Pacific. The population structure and recruitment pattern of both species were studied using modal decomposition of length–frequency distributions. Gastropod populations were collected from Axial Volcano and Endeavour Segment in 2002 and 2003. Polymodal size–frequency distributions, particularly at Axial Volcano vent sites, suggest a discontinuous recruitment pattern for D. globulus. In contrast, there were no distinct peaks visible in the distributions of L. fucensis, suggesting a continuous recruitment pattern for this species. For both species, distributions were positively skewed towards the smaller length–classes, implying post-settlement mortality is high. However, variations in growth, due to short- and long-term variability in environmental conditions in the hydrothermal vent habitat, as well as biological interactions, may also be influencing the distribution and abundance of subsequent life-history stages. Using maximum shell lengths from populations of known ages, the growth rate of L. fucensis was estimated as 9.6 μm day⁻¹, indicating adulthood would be reached in ∼1 year. Our results suggest that, despite occupying the same habitat, abundance and population structure are regulated by different biotic and abiotic processes in L. fucensis and D. globulus.     

Scientists as Stakeholders in Conservation of Hydrothermal Vents

Abstract: Hydrothermal vents are deep‐sea ecosystems that are almost exclusively known and explored by scientists rather than the general public. Continuing scientific discoveries arising from study of hydrothermal vents are concommitant with the increased number of scientific cruises visiting and sampling vent ecosystems. Through a bibliometric analysis, we assessed the scientific value of hydrothermal vents relative to two of the most well‐studied marine ecosystems, coral reefs and seagrass beds. Scientific literature on hydrothermal vents is abundant, of high impact, international, and interdisciplinary and is comparable in these regards with literature on coral reefs and seagrass beds. Scientists may affect hydrothermal vents because their activities are intense and spatially and temporally concentrated in these small systems. The potential for undesirable effects from scientific enterprise motivated the creation of a code of conduct for environmentally and scientifically benign use of hydrothermal vents for research. We surveyed scientists worldwide engaged in deep‐sea research and found that scientists were aware of the code of conduct and thought it was relevant to conservation, but they did not feel informed or confident about the respect other researchers have for the code. Although this code may serve as a reminder of scientists’ environmental responsibilities, conservation of particular vents (e.g., closures to human activity, specific human management) may effectively ensure sustainable use of vent ecosystems for all stakeholders.     

Description and comparison of major foregut ossicles in hydrothermal vent crabs

Major foregut (gastric mill) ossicles, including the dorsal median tooth, lateral teeth, accessory lateral teeth, and cardiopyloric valve, of hydrothermal vent crabs were dissected and examined during the summer of 1996 from specimens housed at the Natural History Museum of Los Angeles County. Ossicles are described for two species of hydrothermal vent crabs (family Bythograeidae Williams, 1980). The western Pacific Austinograea williamsi Hessler and Martin has an unusual dorsal median tooth. The surrounding cuticular flange is scalloped and bears spinulose setae at the tip of each of the protruding edges, a condition perhaps unique in the Brachyura. The lateral teeth are mostly unremarkable, bearing the typical large anterior denticles and deep serrations seen in other crab families, but with a higher number of serrations than is known for any species previously described. The accessory lateral teeth bear flattened, plate-like spines that are widest basally and that taper to a cylindrical tip. The basic armature of the foregut of Bythograea thermydron Williams, known only from vents in the eastern Pacific, is very similar. Scalloping of the median tooth borders is less pronounced, however, and the shape of the tooth itself and of the plate from which it arises is slightly different. The lateral teeth bear fewer and more widely spaced grooves, and the cardiopyloric valve entrance appears less setose at its extremity. Comparison with foregut ossicles in other crab families based on earlier studies, most of which have not employed SEM, reveals some similarities between bythograeids and some xanthids, but does not clarify the phylogenetic position of the bythograeids. Because of the paucity of other SEM studies of the brachyuran foregut, it is difficult to ascertain whether some of the many spine and setal types in the bythograeid foregut are unique or even unusual compared to those of other crab families. Nothing about the foregut of the vent crabs is indicative of their unusual habitat. Anecdotal observations of feeding in vent crabs indicate that they are opportunistic scavengers and omnivores, which is in keeping with the non-specialized nature of the foregut. The debate between adaptation vs phylogeny as determinants of the form of the gastric mill components is briefly discussed. Received: 10 December 1996 / Accepted: 13 November 1997     

Scarred limpets at hydrothermal vents: evidence of predation by deep-sea whelks

The chaotic physical and chemical environment at deep-sea hydrothermal vents has been associated with an ecosystem with few predators, arguably allowing the habitat to provide refuge for vulnerable species. The dominance of endemic limpets with thin, open-coiled shells at north Pacific vents may support this view. To test their vulnerability to predation, the incidence of healed repair scars, which are argued to reflect non-lethal encounters with predators, were examined on the shells of over 5,800 vent limpets of Lepetodrilus fucensis McLean (1988) that were collected from 13 to 18 August 1996. Three vent fields on the Juan de Fuca Ridge at ca. 2,200 m depth were sampled, two within 70 m of 47°56.87′N 129°05.91′W, and one at 47°57.85′N 129°05.15′W with the conspicuous potential limpet predators, the zoarcid fish Pachycara gymninium Anderson and Peden (1988), the galatheid crab Munidopsis alvisca Williams (1988), and the buccinid snail Buccinum thermophilum Harasewych and Kantor (2002). Limpets from the predator-rich vent were most often scarred, a significant difference created by the high incidence of scars on small (<4 mm long) limpets in this sample. Collected with the limpets were small (median shell diameter 4.4 mm) buccinids. They, rather than the larger, more conspicuous mobile fishes and crabs are argued to be the shell-damaging predator. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Vacuolate-attached filaments: highly productive Ridgeia piscesae epibionts at the Juan de Fuca hydrothermal vents

Vacuolate sulfur bacteria with high morphological similarity to vacuolate-attached filaments previously described from shallow hydrothermal vents (White Point, CA) were found at deep-sea hydrothermal vents. These filamentous bacteria grow in dense mats that cover surfaces and potentially provide a significant source of organic carbon where they occur. Vacuolate-attached filaments were collected near vents at the Clam Bed site of the Endeavour Segment of the Juan de Fuca Ridge and from the sediment surface at Escanaba Trough on the Gorda Ridge. A phylogenetic analysis comparing their 16S rRNA gene sequences to those collected from the shallow White Point site showed that all vacuolate-attached filament sequences form a monophyletic group within the vacuolate sulfur-oxidizing bacteria clade in the gamma proteobacteria. Abundance of the attached filaments was quantified over the length of the exterior surface of the tubes of Ridgeia piscesae worms collected from the Clam Bed site at Juan de Fuca yielding a per worm average of 0.070 ± 0.018 cm³ (n = 4). In agreement with previous results for White Point filaments, anion measurements by ion chromatography showed no detectable internal nitrate concentrations above ambient seawater (n = 9). For one R. piscesae tube worm “bush” at the Easter Island vent site, potential gross epibiont productivity is estimated to be 15 to 45× the net productivity of the worms.     

Molecular taxonomy confirms morphological classification of deep-sea hydrothermal vent copepods (Dirivultidae) and suggests broad physiological tolerance of species and frequent dispersal along ridges

Dirivultid copepods are among the most successful organisms at deep-sea hydrothermal vents, as this family includes 50 morphologically described species. We studied COI diversity of some species in various geographical areas and vent fluid regimes, in order to gain a better understanding of true species diversity, dispersal strategies, and evolution. DNA taxonomy revealed the same entities as described with morphological characters. No cryptic species were detected. With the help of COI analyses, it was possible to identify a new species and match the dimorphic sexes of another species. The geographical distance between vents, as well as the extreme physico-chemical environment, are thought to affect the gene flow of fauna. We could not detect any sequence differences within species among different geographical scales (up to 2,000 km) or different vent fluid regimes. We suggest that Dirivultidae have relatively high gene flow between vents and are able to disperse relatively easy along ridges. Further, they have a broad physiological tolerance and thus might not have undergone speciation in response to heterogeneity caused by vent fluids.     

Trophic relationships of hydrothermal vent and non-vent communities in the upper sublittoral and upper bathyal zones off Kueishan Island,Taiwan: a combined morphological,gut content analysis and stable isotope approach

This study used morphological, gut content analysis and carbon- and nitrogen-stable isotope analysis to investigate the trophic structure of upper sublittoral (15–30 m deep) and upper bathyal (200–300 m deep) hydrothermal vents and the adjacent non-vent upper bathyal environment off Kueishan Island. The sublittoral vents host no chemosynthetic fauna, but green and red algae, epibiotic biofilm on crustacean surfaces, and zooplankton form the base of the trophic system. Suspension-feeding sea anemones and the generalist omnivorous vent crab Xenograpsus testudinatus occupy higher trophic levels. The upper bathyal hydrothermal vent is a chemoautotrophic-based system. The vent mussel Bathymodiolus taiwanensis forms a chemosynthetic component of this trophic system. Bacterial biofilm, surface plankton, and algae form the other dietary fractions of the upper bathyal fauna. The vent hermit crab Paragiopagurus ventilatus and the vent crab X. testudinatus are generalist omnivores. The vent-endemic tonguefish Symphurus multimaculatus occupies the top level of the trophic system. The adjacent non-vent upper bathyal region contains decapod crustaceans, which function as either predators or scavengers. The assemblages of X. testudinatus from sublittoral and upper bathyal vents exhibited distinct stable isotope values, suggesting that they feed on different food sources. The upper bathyal Xenograpsus assemblages displayed large variations in their stable isotope values and exhibited an ontogenetic shift in their δ¹³C and δ¹⁵N stable isotope signatures. Some individuals of Xenograpsus exhibited δ¹⁵N values close to those of non-vent species, suggesting that the highly mobile Xenograpsus may transfer energy between the upper bathyal hydrothermal vents and the adjacent non-vent upper bathyal environment.     

Reproductive biology and population structure of the deep-sea hydrothermal vent worm Paralvinella grasslei (Polychaeta: Alvinellidae) at 13°N on the East Pacific Rise

Paralvinella grasslei is a polychaetous annelid living in the harsh, unstable and heterogeneous environmental conditions found at deep-sea hydrothermal vent sites in the eastern Pacific. The aim of this work was to examine the possible influence of the reproductive biology of P. grasslei on the structure of its populations. Maximum observed oocyte size inside the oviduct is 275 m, and fecundity is relatively low. Examination of gametes and young specimens suggested a direct benthic development for this species. The population structure of P. grasslei at 13°N/EPR (EPR=East Pacific Rise) revealed a discontinuous recruitment which seems to be synchronized within vent sites and fields. The data also suggested the occurrence of discrete breeding periods. P. grasslei probably reproduces several times a years, with an apparent periodicity. Tidal signals could be a possible cue for the coordination of the reproductive cycle. The life-history of P. grasslei is discussed in light of the reproductive biology of other terebellomorph polychaetes, and seems to be well adapted for colonizing the unstable environment of hot vents. Two main hypotheses can explain the dissemination processes of this species along axial oceanic ridges. The influence of nearbottom currents occurring along the central graben of the East Pacific Rise can be cosidered to account for part of the transport of larvae and juveniles, but the observations of polychaete erpochaetes on the test of hydrothermal bythograeid crabs and evidence that crab migrations occur between vents also support the possibility of zoochory for the dissemination of alvinellid polychaetes.     

Larvae of benthic invertebrates in hydrothermal vent plumes over Juan de Fuca Ridge

Larvae of benthic invertebrates collected in the water column above Juan de Fuca Ridge show distinct variations in abundance and composition in, and away from, the neutrally-buoyant hydrothermal plume emanating from underlying vents. Larvae of vent gastropods (Lepetodrilus sp. and two peltospirid species) occur in significantly higher abundances in the plume than away from it (mean abundance=21.0 individuals 1000 m^?3 vs 1.4 individuals 1000 m^?3), and larvae of vent bivalves (Calyptogena? sp.) occur exclusively in the plume (mean abundance=0.5 individuals 1000 m^?3). Larvae from other benthic taxa known not to be endemic to Juan de Fuca vent communities, such as anthozoans, pholad clams, bryozoans and echinoderms, are less abundant in the plume than away (mean abundance=47.5 vs 16.9 individuals 1000 m^?3) at comparable depths and heights above the bottom. These results support the hypothesis that larvae of vent species are entrained into buoyant hydrothermal plumes and transported at the level of lateral spreading several hundred meters above the seafloor. The discovery of vent-associated larvae in the plume suggests that models used to predict hydrodynamic processes in the plume will also be useful for modeling larval dispersal. Advanced imaging and new molecular-based approaches will be required to resolve taxonomic uncertainties in some larval groups (e.g. certain polychaete families) in order to distinguish vent species and make comprehensive flux estimates of all vent larvae in the neutrally-buoyant plume.     

The effect of cadmium on antioxidant responses and the susceptibility to oxidative stress in the hydrothermal vent mussel Bathymodiolus azoricus

Hydrothermal vents are a unique environment of extreme physical–chemical characteristics and biological species composition. Cd is a toxic non-essential metal present in high concentrations in the hydrothermal vent environment, contrary to those found in marine coastal areas. Cd toxicity has been related, among other things, with reactive oxygen species production, even though this is a non-redox metal. Bathymodiolus azoricus is a deep-sea Mytilid bivalve very common in the Mid Atlantic Ridge (MAR) hydrothermal vent fields and very little is known about the antioxidant defence system in this specie. Because lethal Cd concentration in B. azoricus is unknown, the aim of this study was to assess the effects of a Cd concentration higher than that found in the hydrothermal vents on oxidative stress biomarkers, such as antioxidant enzymes. Mussels were exposed to 100 μg l⁻¹ Cd during 24, 48 and 144 h, respectively, in a pressurized aquarium (IPOCAMP). Superoxide dismutase (SOD), catalase (CAT), glutathione peroxidases (GPx), total oxyradical scavenging capacity (TOSC), metallothionein (MT) and lipid peroxidation (LPO) were measured in the gills and mantle of B. azoricus. The results indicate that gills are first affected by Cd toxicity. This may be due to different physiological functions of the tissues and by the presence of thio and methanotrophic symbiotic bacteria in the gills. The SOD and CAT are inhibited during the first day of exposure in the gills, although TOSC and MT concentrations were the same in control and exposed mussels. In the mantle, enzymatic activation only occurred after 6 days, and no significant differences in MT concentrations were found in the control and exposed mussels during the first day, as observed in the gills.     

Population structure and reproductive biology of two sympatric hydrothermal vent polychaetes,Paralvinella pandorae and P. palmiformis

The alvinellid polychaetes Paralvinella pandorae Desbruyères and Laubier and P. palmiformis Desbruyères and Laubier occur at deep-sea hydrothermal vents along the Juan de Fuca and Explorer Ridges in the northeast Pacific Ocean. The population structure and reproductive biology of both species were studied in samples taken from three vent sites during six cruises in 1983 and 1984. Size-frequency analyses of two P. pandorae populations produced unimodal histograms, suggesting continuous or semi-continuous juvenile recruitment; in a third population two possible size classes were evident. Histograms of P. palmiformis displayed size-class peaks, which most likely reflected periodic recruitment of juveniles. Both species are gonochoric and gametes develop free in the coelom. Due to the simultaneous presence of a full range of gametogenic stages in P. pandorae populations, including spermatozoa in males, and to the continuous or semi-continuous recruitment pattern suggested by the size-frequency histograms, continuous reproduction is proposed for this species. In P. palmiformis a discrete, possibly synchronized, breeding cycle is thought to occur. Although maximum fecundity of P. pandorae is very low, continual reproduction over a long period of time could enhance its reproductive potential. The estimate of maximum fecundity for P. palmiformis is comparable to estimates for other polychaetes that undergo non-planktotrophic larval development. Maximum observed oocyte size was 215 and 260 m in P. pandorae and P. palmiformis, respectively. It is proposed that P. pandorae broods its young, while P. palmiformis probably undergoes demersal lecithotrophic larval development. The continual production of brooded young by P. pandorae could maintain a vent population, but severely limit dispersal to other vents. Demersal lecithotrophic larvae of P. palmiformis could repopulate vents, and potentially be carried by bottom currents to other vent sites.     

Field distribution and sulphide tolerance of Capitella capitata (Annelida: Polychaeta) around shallow water hydrothermal vents off Milos (Aegean Sea). A new sibling species?

The cosmopolitan polychaete Capitella capitata, known as a complex of opportunistic sibling species, usually dominates the macrobenthos of polluted or unpredictable environments. A population of C. capitata, termed Capitella sp. M, was found in a shallow water hydrothermal vent area south of Milos (Greece). Here, this population occurs close to vent outlets (termed the “transition zone”), an environment with steep gradients of temperature, salinity and pH and increased sulphide concentrations of up to 710 μM. The field distribution of C. capitata in relation to sulphide concentrations around the vent outlets was investigated and sulphide tolerance experiments were conducted on laboratory-cultured worms to elucidate possible adaptations of Capitella sp. M to these extreme environmental conditions. In order to investigate whether the population from the Milos hydrothermal vent area can be considered a distinct sibling species within the C. capitata complex, crossbreeding experiments and analysis of general protein patterns were conducted with Capitella sp. M and three other C. capitata populations of different ecological ranges. Capitella sp. M showed high resistance (median survival time: 107 ± 38 h) to anoxia plus high sulphide concentrations of 740 μM. It seems that the ability to survive high-sulphide conditions in combination with reduced interspecific competition enables the polychaete to maintain a continuous population in this rigorous habitat. From the extremely high tolerance to anoxia and sulphide, shown in both the crossbreeding experiments and the analysis of total proteins, it can be concluded that Capitella sp. M from the Milos hydrothermal vent area represents a separate sibling species within the C. capitata complex. Received: 3 March 1997 / Accepted: 12 September 1997     

Nematode community composition in hydrothermal vent and adjacent non-vent fields around Myojin Knoll,a seamount on the Izu-Ogasawara Arc in the western North Pacific Ocean

In contrast to specific large benthic invertebrates in chemosynthetic ecosystems such as hydrothermal vents, meiofaunal communities in such habitats have been reported to have strong taxonomic overlap with meiofauna in the adjacent “normal” environments. However, meiofauna have only recently been included in studies of those environments and detailed information on these communities is still rare. This is especially true in the Northwest Pacific Ocean, even though there are many seamounts with active vents in the calderas of the region. Nematode community composition at the genus level in sediments from a hydrothermal vent field in the caldera of Myojin Knoll (32°06′N, 139°52′E, depth 1,300 m), a seamount on the Izu-Ogasawara Arc, Japan, was investigated for the first time and was compared with adjacent non-vent areas inside and outside the caldera. Multivariate analyses showed that the composition of nematodes in the hydrothermal field was significantly different from that in the non-hydrothermal fields around the caldera. However, the common genera, such as Oxystomina, Pareudesmoscolex, Desmoscolex, and Microlaimus were found in two, or all three vent fields while their rank contributions differed among the three fields. When the data from Myojin Knoll were compared with those from other deep-sea vent environments in different regions (e.g., North Fiji Basin, East Pacific Rise, Mid-Atlantic Ridge), the nematode composition in the vent field of the Myojin caldera was more similar to that of the non-vent fields around the caldera than the composition in vent fields of other regions. These data from the Northwest Pacific Ocean also suggest the absence of long-range transport systems and local adaptations for meiofauna in hydrothermal vent fields.     

A new bathymodioline mussel symbiosis at the Juan de Fuca hydrothermal vents

Until recently, the only major hydrothermal vent biogeographic province not known to include bathymodioline mussels was the spreading centers of the northeast Pacific, but deep-sea dives using DSV Alvin on the Endeavor segment of the Juan de Fuca Ridge (47°56N 129°06W; ∼2,200 m depth) in August 1999 yielded the only recorded bathymodioline mytilids from these northeastern Pacific vents. One specimen in good condition was evaluated for its relatedness to other deep-sea bathymodioline mussels and for the occurrence of chemoautotrophic and/or methanotrophic symbionts in the gills. Phylogenetic analyses of the host cytochrome oxidase I gene show this mussel shares evolutionary alliances with hydrothermal vent and cold seep mussels from the genus Bathymodiolus, and is distinct from other known species of deep-sea bathymodiolines, suggesting this mussel is a newly discovered species. Ultrastructural analyses of gill tissue revealed the presence of coccoid bacteria that lacked the intracellular membranes observed in methanotrophic symbionts. The bacteria may be extracellular but poor condition of the fixed tissue complicated conclusions regarding symbiont location. A single gamma-proteobacterial 16S rRNA sequence was amplified from gill tissue and directly sequenced from gill tissue. This sequence clusters with other mussel chemoautotrophic symbiont 16S rRNA sequences, which suggests a chemoautotrophic, rather than methanotrophic, symbiosis in this mussel. Stable carbon (δ¹³C = −26.6%) and nitrogen (δ¹⁵N = +5.19%) isotope ratios were also consistent with those reported for other chemoautotroph-mussel symbioses. Despite the apparent rarity of these mussels at the Juan de Fuca vent sites, this finding extends the range of the bathymodioline mussels to all hydrothermal vent biogeographic provinces studied to date.     

Origin of the antitropical distribution pattern in marine mussels (Mytilus spp.): routes and timing of transequatorial migration

Many marine species, including mussels in the Mytilus edulis species group (i.e. M. edulis L., M. galloprovincialis Lamarck, and M. trossulus Gould), have an antitropical distribution pattern, with closely related taxa occurring in high latitudes of the northern and southern hemispheres but being absent from the tropics. We tested four hypotheses to explain the timing and route of transequatorial migration by species with antitropical distributions. These hypotheses yield different predictions for the phylogenetic relationship of southern hemisphere taxa relative to their northern counter-parts. The three Mytilus species were used to test these hypotheses since they exhibit a typical antitropical distribution and representative taxa occur in both the Pacific and Atlantic. Two types of mtDNA lineages were found among populations of mussels collected from the southern hemisphere between 1988 and 1996; over 90% of the mtDNA lineages formed a distinct subclade which, on average, had 1.4% divergence from haplotypes found exclusively in northern Atlantic populations of M. galloprovincialis. These data indicate that southern hemisphere mussels arose from a migration event from the northern hemisphere during the Pleistocene via an Atlantic route. The remainder of the southern hemisphere lineages (<10%) were very closely related to mtDNA haplotypes found in both M. edulis and M. galloprovincialis in the northern hemisphere, suggesting a second, more recent migration to the southern hemisphere. There was no evidence that southern hemisphere mussels arose from Pacific populations of mussels. Received: 8 December 1998 / Accepted: 8 November 1999     

Persistence,morphology, and nutritional state of a gastropod hosted bacterial symbiosis in different levels of hydrothermal vent flux

The limpet, Lepetodrilus fucensis McLean, is found in prominent stacks around hydrothermal vents on the Juan de Fuca Ridge. L. fucensis hosts a filamentous episymbiont on its gill lamellae that may be ingested directly by the gill epithelium. To assess the persistence of this symbiosis I used microscopy to examine the gills of L. fucensis from sites representing its geographic range and different habitats. The symbiosis is present on all the specimens examined in this study, including both sexes and a range of juvenile and adult sizes. Next, I aimed to determine if patterns in bacterial abundance, host condition, and gill morphology support the hypotheses that the bacteria are chemoautotrophic and provide limpets with a food resource. To do so, I compared specimens from high and low flux locations at multiple vents. My results support the above hypotheses: (1) gill bacteria are significantly less abundant in low flux where the concentrations of reduced chemicals (for chemoautotrophy) are negligible, (2) low flux specimens have remarkably poor tissue condition, and (3) the lamellae of high flux limpets have greater surface area: the blood space and bacteria-hosting epithelium are deeper and have more folds than low flux lamellae, modifications that support higher symbiont abundances. I next asked if the morphology of the lamellae could change. To test this, I moved high flux limpets away from a vent and after 1 year the lamellar depth and shape of the transplanted specimens resembled low flux gills. Last, I was interested in whether bacterial digestion by the gill epithelium is a significant feeding mechanism. As bacteria-like cells are rarely apparent in lysosomes of the gill epithelium, I predicted that lysosome number would be unrelated to bacterial abundance. My data support this prediction, suggesting that digestion of bacteria by the gill epithelium probably contributes only minimally to the limpet’s nutrition. Overall, the persistence and morphology of the L. fucensis gill symbiosis relates to the intensity of vent flux and indicates that specimens from a variety of habitats may be necessary to characterize the morphological variability of gill-hosted symbioses in other molluscs.     

Reproductive traits of pioneer gastropod species colonizing deep-sea hydrothermal vents after an eruption

The colonization dynamics and life histories of pioneer species determine early succession at nascent hydrothermal vents, and their reproductive ecology may provide insight into their dispersal and population connectivity. Studies on the reproductive traits of two pioneer gastropod species, Ctenopelta porifera and Lepetodrilus tevnianus, began within a year after an eruption on the East Pacific Rise (EPR) that eliminated vent communities near 9°50′N from late 2005/early 2006. Standard histology was used to examine gamete release, instantaneous female fecundity, and time to maturation. Both species exhibited two-component oocyte size–frequency distributions indicating quasi-continuous reproduction with high fecundity. In samples collected in December 2006, both C. porifera and L. tevnianus individuals were reproductively mature. The smallest reproducing C. porifera were 4.2 mm (males) and 5.4 mm (females) in shell length, whereas reproductive L. tevnianus were smaller (2.3 and 2.4 mm in males and females, respectively). Most C. porifera were large (>6.0 mm) compared to their size at metamorphosis and reproductively mature. In contrast, most L. tevnianus were small (<1.0 mm) and immature. Reproductive traits of the two species are consistent with opportunistic colonization, but are also similar to those of other Lepetodrilus species and peltospirids at vents and do not fully explain why these particular species were the dominant pioneers. Their larvae were probably in high supply immediately after the eruption, due to oceanographic transport processes from remote source populations.