Expanding dispersal studies at hydrothermal vents through species identification of cryptic larval forms

Author Posting. © The Author(s), 2010. This is the author's version of the work. It is posted here by permission of Springer for personal use, not for redistribution. The definitive version was published in Marine Biology 157 (2010): 1049-1062, doi:10.1007/s00227-009-1386-8.The rapid identification of hydrothermal vent-endemic larvae to the species level is a key limitation to understanding the dynamic processes that control the abundance and distribution of fauna in such a patchy and ephemeral environment. Many larval forms collected near vents, even those in groups such as gastropods that often form a morphologically distinct larval shell, have not been identified to species. We present a staged approach that combines morphological and molecular identification to optimize the capability, efficiency, and economy of identifying vent gastropod larvae from the northern East Pacific Rise (NEPR). With this approach, 15 new larval forms can be identified to species. A total of 33 of the 41 gastropod species inhabiting the NEPR, and 26 of the 27 gastropod species known to occur specifically in the 9° 50’ N region, can be identified to species. Morphological identification efforts are improved by new protoconch descriptions for Gorgoleptis spiralis, Lepetodrilus pustulosus, Nodopelta subnoda, and Echinopelta fistulosa. Even with these new morphological descriptions, the majority of lepetodrilids and peltospirids require molecular identification. Restriction fragment length polymorphism digests are presented as an economical method for identification of five species of Lepetodrilus and six species of peltospirids. The remaining unidentifiable specimens can be assigned to species by comparison to an expanded database of 18S ribosomal DNA. The broad utility of the staged approach was exemplified by the revelation of species-level variation in daily planktonic samples and the identification and characterization of egg capsules belonging to a conid gastropod Gymnobela sp. A. The improved molecular and morphological capabilities nearly double the number of species amenable to field studies of dispersal and population connectivity.Funding was provided by as Woods Hole Oceanographic Institution Deep Ocean Exploration Institute grant to L.M and S. Beaulieu, National Science Foundation grants OCE-0424953, OCE-9712233, and OCE-9619605 to L.M, OCE-0327261 to T.S., and OCE-0002458 to K. Von Damm, and a National Defense Science and Engineering Graduate fellowship to D.A

High environmental stress and productivity increase functional diversity along a deep‐sea hydrothermal vent gradient

peer reviewedProductivity and environmental stress are major drivers of multiple biodiversity facets and faunal community structure. Little is known on their interacting effects on early community assembly processes in the deep sea (>200 m), the largest environment on Earth. However, at hydrothermal vents productivity correlates, at least partially, with environmental stress. Here, we studied the colonization of rock substrata deployed along a deep‐sea hydrothermal vent gradient at four sites with and without direct influence of vent fluids at 1,700‐m depth in the Lucky Strike vent field (Mid‐Atlantic Ridge [MAR]). We examined in detail the composition of faunal communities (>20 μm) established after 2 yr and evaluated species and functional patterns. We expected the stressful hydrothermal activity to (1) limit functional diversity and (2) filter for traits clustering functionally similar species. However, our observations did not support our hypotheses. On the contrary, our results show that hydrothermal activity enhanced functional diversity. Moreover, despite high species diversity, environmental conditions at surrounding sites appear to filter for specific traits, thereby reducing functional richness. In fact, diversity in ecological functions may relax the effect of competition, allowing several species to coexist in high densities in the reduced space of the highly productive vent habitats under direct fluid emissions. We suggest that the high productivity at fluid‐influenced sites supports higher functional diversity and traits that are more energetically expensive. The presence of exclusive species and functional entities led to a high turnover between surrounding sites. As a result, some of these sites contributed more than expected to the total species and functional β diversities. The observed faunal overlap and energy links (exported productivity) suggest that rather than operating as separate entities, habitats with and without influence of hydrothermal fluids may be considered as interconnected entities. Low functional richness and environmental filtering suggest that surrounding areas, with their very heterogeneous species and functional assemblages, may be especially vulnerable to environmental changes related to natural and anthropogenic impacts, including deep‐sea mining

Do Larval Supply and Recruitment Vary among Chemosynthetic Environments of the Deep Sea?

BACKGROUND: The biological communities that inhabit chemosynthetic environments exist in an ephemeral and patchily distributed habitat with unique physicochemical properties that lead to high endemicity. Consequently, the maintenance and recovery from perturbation of the populations in these habitats is, arguably, mainly regulated by larval supply and recruitment. METHODOLOGY/PRINCIPAL FINDINGS: WE USE DATA FROM THE PUBLISHED SCIENTIFIC LITERATURE TO: (1) compare the magnitudes of and variability in larval supply and settlement and recruitment at hydrothermal vents, seeps, and whale, wood and kelp falls; (2) explore factors that affect these life history processes, when information is available; and (3) explore taxonomic affinities in the recruit assemblages of the different chemosynthetic habitats, using multivariate statistical techniques. Larval supply at vents can vary across segments by several orders of magnitude for gastropods; for bivalves, supply is similar at vents on different segments, and at cold seeps. The limited information on larval development suggests that dispersal potential may be highest for molluscs from cold seeps, intermediate for siboglinids at vents and lowest for the whale-bone siboglinid Osedax. Settlement is poorly studied and only at vents and seeps, but tends to be highest near an active source of emanating fluid in both habitats. Rate of recruitment at vents is more variable among studies within a segment than among segments. Across different chemosynthetic habitats, recruitment rate of bivalves is much more variable than that of gastropods and polychaetes. Total recruitment rate ranges only between 0.1 and 1 ind dm(-2) d(-1) across all chemosynthetic habitats, falling above rates in the non-reducing deep sea. The recruit assemblages at vents, seeps and kelp falls have lower taxonomic breadth, and include more families and genera that have many species more closely related to each other than those at whale and wood falls. Vents also have the most uneven taxonomic structure, with fewer recruits represented by higher taxonomic levels (phyla, orders, classes) compared to seeps and wood and kelp falls, whereas the opposite is true at whale falls. CONCLUSIONS/SIGNIFICANCE: Based on our evaluation of the literature, the patterns and regulatory factors of the early history processes in chemosynthetic environments in the deep sea remain poorly understood. More research focused on these early life history stages will allow us to make inferences about the ecological and biogeographic linkages among the reducing habitats in the deep sea

Panmixia in a fragmented and unstable environment: the hydrothermal shrimp Rimicaris exoculata disperses extensively along the Mid-Atlantic ridge

Dispersal plays a fundamental role in the evolution and persistence of species, and especially for species inhabiting extreme, ephemeral and highly fragmented habitats as hydrothermal vents. The Mid-Atlantic Ridge endemic shrimp species Rimicaris exoculata was studied using microsatellite markers to infer connectivity along the 7100-Km range encompassing the sampled sites. Astonishingly, no genetic differentiation was found between individuals from the different geographic origins, supporting a scenario of widespread large-scale dispersal despite the habitat distance and fragmentation. We hypothesize that delayed metamorphosis associated to temperature differences or even active directed migration dependent on physical and/or chemical stimuli could explain these results and warrant further studies on adaptation and dispersal mechanisms

Species identification of marine invertebrate early stages by whole-larvae in situ hybridisation of 18S ribosomal RNA

The ability to identify early life-history stages of organisms is essential for a better understanding of population dynamics and for attempts to inventory biodiversity. The morphological identification of larvae is time consuming and often not possible in those species with early life-history stages that are radically different from their adult counterparts. Molecular methods have been successful in identifying marine larvae; however, to date these methods have been destructive. We describe here an in situ hybridisation (ISH) technique that uses oligonucleotide probes specific for the 18S ribosomal RNA gene to identify marine larvae. Our technique leaves the larvae intact, thus allowing the description of larvae whose morphology was not previously known. Only 1 mismatch between the rRNA sequences of target and non-target species is sufficient to discriminate species, with nearly 100% efficiency. We developed a colourimetric assay that can be detected with a dissecting microscope, and is thus suitable for autofluorescent or large eggs and larvae that cannot be sorted under a microscope. Probe binding is revealed by an enzymatic reaction catalysed by either a horseradish peroxidase or an alkaline phosphatase. ISH was broadly applicable: it was effective in identifying eggs, larvae and adult tissues, soft-bodied larvae (polychaetes) and larvae with hard shells (bivalves), larvae belonging to different phyla and from different environments. Further advantages of this method are its relatively low cost, that only a minimal amount of equipment is needed, and that 100s of specimens can be processed quickly and simultaneously

Development of assemblages associated with alvinellid colonies on the walls of high-temperature vents at the East Pacific Rise

Symposium on Marine Benthic Ecology and Biodiversity - A Compilation of Recent Advances held in Honor of J Frederick Grassle, Rutgers Univ, Inst Marine Coastal Sci, New Brunswick, NJ, NOV 20-21, 2008International audienceSeveral species of the polychaete family Alvinellidae may be considered as `ecosystem engineer' because, by building their tubes, they modify the architecture of the hydrothermal fluid-seawater interface on the walls of vent chimneys. This affects the thermal and chemical gradients, and creates a mosaic of micro-niches, which could enable colonization by a variety of less-tolerant species. On high temperature vents of the Juan de Fuca Ridge, Alvinellid-dominated communities colonizing first mineral surfaces are followed by a succession of communities with different species composition. On the East Pacific Rise (EPR), tubes of Alvinella spp, may seal the mineral surface on which they grow and decrease fluid seepage, or tubes may become encrusted in mineral precipitations. An alvinellid colony may therefore persist for only a restricted time period at a given place. Here we investigated the development of alvinellid colonies on the EPR vent sites in order to detect whether a succession of new species less tolerant would follow colonization by Alvinella spp. or if different assemblages are forming depending on local conditions. Using a specially designed device called TRAC (titanium ring for alvinellid colonization), we described the evolution of newly formed colonies. Fifteen experiments were conducted on several chimneys of the 9 degrees N and 13 degrees N vent fields of the EPR, over durations ranging from 5 days up to 5 months. Through video analysis, different types of colonies were identified, characterized by increasing thickness of the Alvinella coverage, decreasing fluid flow bathing the colony, and decreasing surface temperatures. We showed that the assemblage formed by minerals, tubes, and organisms is produced at a very high rate. While animals may colonize the new surface in less than a week, and tubes are also quickly produced (Alvinella species may grow their tube up to 1 cm day(-1) during the early stages of colonization), mineral precipitation progressively increases the mineral content of the assemblage. Active colonies do not seem to persist longer than 5 months, highlighting the rapid turnover of this habitat. Colonies collected had different species compositions, but community structures exhibited no significant variations with vent field (9 degrees N/13 degrees N), deployment duration ( 1 month), or type of colony. However, multivariate analysis revealed that mineral content would best explain community structure variations. Biodiversity indexes increased quickly within the first weeks of TRAC deployment time, as well as with the amount of Alvinella tube. The development of a complex architecture may thus promote the installation of species lacking adaptations to temperature. However, our results do not support a succession pattern but rather the development of communities with slight differences in species compositions that may reflect local environmental conditions. (C) 2009 Elsevier Ltd. All rights reserved