Parasite diversity at isolated, disturbed hydrothermal vents.

Habitat isolation and disturbance are important regulators of biodiversity, yet it remains unclear how these environmental features drive differences in parasite diversity between ecosystems. We test whether the biological communities in an isolated, frequently disturbed marine ecosystem (deep-sea hydrothermal vents) have reduced parasite richness and relatively fewer parasite species with indirect life cycles (ILCs) compared to ecosystems that are less isolated and less disturbed. We surveyed the parasite fauna of the biological community at the 9°50'N hydrothermal vent field on the East Pacific Rise and compared it to similar datasets from a well-connected and moderately disturbed ecosystem (kelp forest) and an isolated and undisturbed ecosystem (atoll sandflat). Parasite richness within host species did not differ significantly between ecosystems, yet total parasite richness in the vent community was much lower due to the low number of predatory fish species. Contrary to expectation, the proportion of ILC parasite species was not lower at vents due to a high richness of trematodes, while other ILC parasite taxa were scarce (nematodes) or absent (cestodes). These results demonstrate the success of diverse parasite taxa in an extreme environment and reinforce the importance of host diversity and food web complexity in governing parasite diversity.

Responding to the signal and the noise: behavior of planktonic gastropod larvae in turbulence.

Swimming organisms may actively adjust their behavior in response to the flow around them. Ocean flows are typically turbulent and are therefore characterized by chaotic velocity fluctuations. While some studies have observed planktonic larvae altering their behavior in response to turbulence, it is not always clear whether a plankter is responding to an individual turbulence fluctuation or to the time-averaged flow. To distinguish between these two paradigms, we conducted laboratory experiments with larvae in turbulence. We observed veliger larvae of the gastropod Crepidula fornicata in a jet-stirred turbulence tank while simultaneously measuring two components of the fluid and larval velocity. Larvae were studied at two different stages of development, early and late, and their behavior was analyzed in response to different characteristics of turbulence: acceleration, dissipation and vorticity. Our analysis considered the effects of both the time-averaged flow and the instantaneous flow, around the larvae. Overall, we found that both stages of larvae increased their upward swimming speeds in response to increasing turbulence. However, we found that the early-stage larvae tended to respond to the time-averaged flow, whereas the late-stage larvae tended to respond to the instantaneous flow around them. These observations indicate that larvae can integrate flow information over time and that their behavioral responses to turbulence can depend on both their present and past flow environments.

Departures from isotropy: the kinematics of a larval snail in response to food.

The swimming behavior of invertebrate larvae can affect their dispersal, survival and settlement in the ocean. Modeling this behavior accurately poses unique challenges as behavior is controlled by both physiology and environmental cues. Some larvae use cilia to both swim and create feeding currents, resulting in potential trade-offs between the two functions. Food availability is naturally patchy and often occurs in shallow horizontal layers in the ocean. Also, larval swimming motions generally differ in the horizontal and vertical directions. In order to investigate behavioral response to food by ciliated larvae, we measured their behavioral anisotropy by quantifying deviations from a model based on isotropic diffusion. We hypothesized that larvae would increase horizontal swimming and decrease vertical swimming after encountering food, which could lead to aggregation at food layers. We considered Crepidula fornicata larvae, which are specifically of interest as they exhibit unsteady and variable swimming behaviors that are difficult to categorize. We tracked the larvae in still water with and without food, with a portion of the larvae starved beforehand. On average, larvae in the presence of food were observed higher in the water column, with higher swimming speeds and higher horizontal swimming velocities when compared with larvae without food. Starved larvae also exhibited higher vertical velocities in food, suggesting no aggregation behavior. Although most treatments showed strong anisotropy in larval behavior, we found that starved larvae without food exhibited approximately isotropic kinematics, indicating that behavioral anisotropy can vary with environmental history and conditions to enhance foraging success or mitigate food-poor environments.

Ontogenetic changes in larval swimming and orientation of pre-competent sea urchin Arbacia punctulata in turbulence.

Many marine organisms have complex life histories, having sessile adults and relying on the planktonic larvae for dispersal. Larvae swim and disperse in a complex fluid environment and the effect of ambient flow on larval behavior could in turn impact their survival and transport. However, to date, most studies on larvae-flow interactions have focused on competent larvae near settlement. We examined the importance of flow on early larval stages by studying how local flow and ontogeny influence swimming behavior in pre-competent larval sea urchins, Arbacia punctulata We exposed larval urchins to grid-stirred turbulence and recorded their behavior at two stages (4- and 6-armed plutei) in three turbulence regimes. Using particle image velocimetry to quantify and subtract local flow, we tested the hypothesis that larvae respond to turbulence by increasing swimming speed, and that the increase varies with ontogeny. Swimming speed increased with turbulence for both 4- and 6-armed larvae, but their responses differed in terms of vertical swimming velocity. 4-Armed larvae swam most strongly upward in the unforced flow regime, while 6-armed larvae swam most strongly upward in weakly forced flow. Increased turbulence intensity also decreased the relative time that larvae spent in their typical upright orientation. 6-Armed larvae were tilted more frequently in turbulence compared with 4-armed larvae. This observation suggests that as larvae increase in size and add pairs of arms, they are more likely to be passively re-oriented by moving water, rather than being stabilized (by mechanisms associated with increased mass), potentially leading to differential transport. The positive relationship between swimming speed and larval orientation angle suggests that there was also an active response to tilting in turbulence. Our results highlight the importance of turbulence to planktonic larvae, not just during settlement but also in earlier stages through morphology-flow interactions.

Larvae from afar colonize deep-sea hydrothermal vents after a catastrophic eruption.

The planktonic larval stage is a critical component of life history in marine benthic species because it confers the ability to disperse, potentially connecting remote populations and leading to colonization of new sites. Larval-mediated connectivity is particularly intriguing in deep-sea hydrothermal vent communities, where the habitat is patchy, transient, and often separated by tens or hundreds of kilometers. A recent catastrophic eruption at vents near 9 degrees 50'N on the East Pacific Rise created a natural clearance experiment and provided an opportunity to study larval supply in the absence of local source populations. Previous field observations have suggested that established vent populations may retain larvae and be largely self-sustaining. If this hypothesis is correct, the removal of local populations should result in a dramatic change in the flux, and possibly species composition, of settling larvae. Fortuitously, monitoring of larval supply and colonization at the site had been established before the eruption and resumed shortly afterward. We detected a striking change in species composition of larvae and colonists after the eruption, most notably the appearance of the gastropod Ctenopelta porifera, an immigrant from possibly more than 300 km away, and the disappearance of a suite of species that formerly had been prominent. This switch demonstrates that larval supply can change markedly after removal of local source populations, enabling recolonization via immigrants from distant sites with different species composition. Population connectivity at this site appears to be temporally variable, depending not only on stochasticity in larval supply, but also on the presence of resident populations.

Functional traits provide new insight into recovery and succession at deep-sea hydrothermal vents.

Investigation of communities in extreme environments with unique conditions has the potential to broaden or challenge existing theory as to how biological communities assemble and change through succession. Deep-sea hydrothermal vent ecosystems have strong, parallel gradients of nutrients and environmental stress, and present unusual conditions in early succession, in that both nutrient availability and stressors are high. We analyzed the succession of the invertebrate community at 9°50' N on the East Pacific Rise for 11 yr following an eruption in 2006 in order to test successional theories developed in other ecosystems. We focused on functional traits including body size, external protection, provision of habitat (foundation species), and trophic mode to understand how the unique nutritional and stress conditions influence community composition. In contrast to established theory, large, fast-growing, structure-forming organisms colonized rapidly at vents, while small, asexually reproducing organisms were not abundant until later in succession. Species in early succession had high external protection, as expected in the harsh thermal and chemical conditions after the eruption. Changes in traits related to feeding ecology and dispersal potential over succession agreed with expectations from other ecosystems. We also tracked functional diversity metrics over time to see how they compared to species diversity. While species diversity peaked at 8 yr post-eruption, functional diversity was continuing to increase at 11 yr. Our results indicate that deep-sea hydrothermal vents have distinct successional dynamics due to the high stress and high nutrient conditions in early succession. These findings highlight the importance of extending theory to new systems and considering function to allow comparison between ecosystems with different species and environmental conditions.

Larvae of Deep-Sea Invertebrates Harbor Low-Diversity Bacterial Communities.

AbstractMicrobial symbionts are a common life-history character of marine invertebrates and their developmental stages. Communities of bacteria that associate with the eggs, embryos, and larvae of coastal marine invertebrates tend to be species specific and correlate with aspects of host biology and ecology. The richness of bacteria associated with the developmental stages of coastal marine invertebrates spans four orders of magnitude, from single mutualists to thousands of unique taxa. This understanding stems predominately from the developmental stages of coastal species. If they are broadly representative of marine invertebrates, then we may expect deep-sea species to associate with bacterial communities that are similar in diversity. To test this, we used amplicon sequencing to profile the bacterial communities of invertebrate larvae from multiple taxonomic groups (annelids, molluscs, crustaceans) collected from 2500 to 3670 m in depth in near-bottom waters near hydrothermal vents in 3 different regions of the Pacific Ocean (the East Pacific Rise, the Mariana Back-Arc, and the Pescadero Basin). We find that larvae of deep-sea invertebrates associate with low-diversity bacterial communities (~30 bacterial taxa) that lack specificity between taxonomic groups. The diversity of these communities is estimated to be ~7.9 times lower than that of coastal invertebrate larvae, but this result depends on the taxonomic group. Associating with a low-diversity community may imply that deep-sea invertebrate larvae do not have a strong reliance on a microbiome and that the hypothesized lack of symbiotic contributions would differ from expectations for larvae of coastal marine invertebrates.

Imprint of past environmental regimes on structure and succession of a deep-sea hydrothermal vent community.

Dramatic perturbations of ecological communities through rapid shifts in environmental regime do not always result in complete mortality of residents. Instead, legacy individuals may remain and influence the succession and composition of subsequent communities. We used a reciprocal transplant experiment to investigate whether a legacy effect is detectable in communities experiencing an abrupt increase or decrease in hydrothermal fluid flux at deep-sea vents. Vent habitats are characterized by strong gradients in productivity and physico-chemical stressors, both of which tend to increase with increasing vent fluid flux. In our experiments, many species survived transplantation from cool (water temperatures <2 degrees C above ambient) to warm (4-30 degrees C above ambient) habitats, resulting in significantly higher species richness on transplanted than remaining experimental substrata. A legacy effect was much less apparent in transplantation from warm to cool habitat, although a few vestimentiferan tubeworms, normally restricted to warm habitat, survived transplantation. The asymmetry in influence of legacy individuals suggests that productivity enhancement may outweigh potential physiological stress in setting limits to distributions of vent invertebrates. This influence of biological processes contrasts with theory developed in the rocky intertidal that predicts the predominance of physical control at the high-stress end of an environmental gradient. Prediction of successional transitions in vents and other habitats experiencing regime shifts in which remnant species may survive must take into account the possible influence of historical effects.

Assessment of the Cape Cod phylogeographic break using the bamboo worm Clymenella torquata reveals the role of regional water masses in dispersal.

Previous genetic studies suggest Cape Cod, MA, as a phylogenetic break for benthic marine invertebrates; however, diffuse sampling in this area has hindered fine-scale determination of the break's location and underlying causes. Furthermore, some species exhibit breaks in different places, and others exhibit no breaks in this region. We analyze the phylogeographic patterns of 2 mitochondrial genes from 10 populations of the bamboo worm Clymenella torquata (Annelida: Maldanidae) focused around Cape Cod but extending from the Bay of Fundy, Canada, to New Jersey. A common invertebrate along the US coast, C. torquata, possesses life-history characteristics that should make it sensitive to factors such as dispersal barriers, bottlenecks, and founder events. As an inhabitant of soft sediments, C. torquata offers a unique contrast to existing research dominated by organisms dwelling on hard substrates. Our genetic data show a clear phylogenetic break and a cline of haplotype frequencies from north to south. Fine-scale sampling of populations on Cape Cod, combined with other sampled populations, confirm that this distinct break is not on the Cape Cod peninsula itself but to the south near a boundary of oceanic water masses. Low levels of gene flow occur in these populations, in an asymmetric manner congruent with coastal current patterns. No significant effect of Pleistocene glaciation was seen in the pattern of genetic diversity over the sampled range.

Habitat associations in gastropod species at East Pacific Rise hydrothermal vents (9 degrees 50'N).

At deep-sea hydrothermal vents on the East Pacific Rise (9 degrees 50'N), distinct megafaunal assemblages are positioned along strong thermal and chemical gradients. We investigated the distribution of gastropod species to determine whether they associate with specific megafaunal zones and to determine the thermal boundaries of their habitats. Gastropods colonized a series of basalt blocks that were placed into three different zones characterized by vestimentiferan tubeworms, bivalves, and suspension-feeders, respectively. Additional gastropods were collected on selected blocks from higher temperature vestimentiferan habitat and from grab samples of alvinellid polychaetes. On the blocks, gastropod species clustered into a "Cool" group (Clypeosectus delectus, Eulepetopsis vitrea, Gorgoleptis spiralis, and Lepetodrilus ovalis) whose species tended to be most abundant in the suspension-feeder zone, and a "Warm" group (Lepetodrilus cristatus, L. elevatus, L. pustulosus, and Cyathermia naticoides) whose species all were significantly more abundant in the vestimentiferan zone than elsewhere. The temperature ranges of Cool species were generally lower than the ranges of Warm ones, although both groups were present at 3 to 6 degrees C; also present was Bathymargarites symplector, which clustered with neither group. Three additional species, Rhynchopelta concentrica, Neomphalus fretterae, and Nodopelta rigneae, co-occurred with Warm-group species on selected blocks from hotter habitats. Although a few species were found only in alvinellid collections, most species were not exclusive to a specific megafaunal zone. We propose that species in the Cool and Warm groups occupy specific microhabitats that are present in more than one zone.

Early exposure of bay scallops (Argopecten irradians) to high CO2 causes a decrease in larval shell growth.

Ocean acidification, characterized by elevated pCO2 and the associated decreases in seawater pH and calcium carbonate saturation state (Ω), has a variable impact on the growth and survival of marine invertebrates. Larval stages are thought to be particularly vulnerable to environmental stressors, and negative impacts of ocean acidification have been seen on fertilization as well as on embryonic, larval, and juvenile development and growth of bivalve molluscs. We investigated the effects of high CO2 exposure (resulting in pH = 7.39, Ω(ar) = 0.74) on the larvae of the bay scallop Argopecten irradians from 12 h to 7 d old, including a switch from high CO2 to ambient CO2 conditions (pH = 7.93, Ω(ar) = 2.26) after 3 d, to assess the possibility of persistent effects of early exposure. The survival of larvae in the high CO2 treatment was consistently lower than the survival of larvae in ambient conditions, and was already significantly lower at 1 d. Likewise, the shell length of larvae in the high CO2 treatment was significantly smaller than larvae in the ambient conditions throughout the experiment and by 7 d, was reduced by 11.5%. This study also demonstrates that the size effects of short-term exposure to high CO2 are still detectable after 7 d of larval development; the shells of larvae exposed to high CO2 for the first 3 d of development and subsequently exposed to ambientCO2 were not significantly different in size at 3 and 7 d than the shells of larvae exposed to high CO2 throughout the experiment.

Detecting the influence of initial pioneers on succession at deep-sea vents.

Deep-sea hydrothermal vents are subject to major disturbances that alter the physical and chemical environment and eradicate the resident faunal communities. Vent fields are isolated by uninhabitable deep seafloor, so recolonization via dispersal of planktonic larvae is critical for persistence of populations. We monitored colonization near 9°50'N on the East Pacific Rise following a catastrophic eruption in order to address questions of the relative contributions of pioneer colonists and environmental change to variation in species composition, and the role of pioneers at the disturbed site in altering community structure elsewhere in the region. Pioneer colonists included two gastropod species: Ctenopelta porifera, which was new to the vent field, and Lepetodrilus tevnianus, which had been rare before the eruption but persisted in high abundance afterward, delaying and possibly out-competing the ubiquitous pre-eruption congener L. elevatus. A decrease in abundance of C. porifera over time, and the arrival of later species, corresponded to a decrease in vent fluid flow and in the sulfide to temperature ratio. For some species these successional changes were likely due to habitat requirements, but other species persisted (L. tevnianus) or arrived (L. elevatus) in patterns unrelated to their habitat preferences. After two years, disturbed communities had started to resemble pre-eruption ones, but were lower in diversity. When compared to a prior (1991) eruption, the succession of foundation species (tubeworms and mussels) appeared to be delayed, even though habitat chemistry became similar to the pre-eruption state more quickly. Surprisingly, a nearby community that had not been disturbed by the eruption was invaded by the pioneers, possibly after they became established in the disturbed vents. These results indicate that the post-eruption arrival of species from remote locales had a strong and persistent effect on communities at both disturbed and undisturbed vents.

Surface-generated mesoscale eddies transport deep-sea products from hydrothermal vents.

Atmospheric forcing, which is known to have a strong influence on surface ocean dynamics and production, is typically not considered in studies of the deep sea. Our observations and models demonstrate an unexpected influence of surface-generated mesoscale eddies in the transport of hydrothermal vent efflux and of vent larvae away from the northern East Pacific Rise. Transport by these deep-reaching eddies provides a mechanism for spreading the hydrothermal chemical and heat flux into the deep-ocean interior and for dispersing propagules hundreds of kilometers between isolated and ephemeral communities. Because the eddies interacting with the East Pacific Rise are formed seasonally and are sensitive to phenomena such as El Niño, they have the potential to introduce seasonal to interannual atmospheric variations into the deep sea.