Susan W. Mills

PREDATION STRUCTURES COMMUNITIES AT DEEP-SEA HYDROTHERMAL VENTS

The structure and dynamics of natural communities result from the interplay of abiotic and biotic factors. We used manipulative field experiments to determine the relative roles of abiotic conditions and biotic interactions in structuring deep-sea (2500 m depth) communities along environmental gradients around hydrothermal vents of the eastern tropical Pacific Ocean (East Pacific Rise, at 9 50 N). We tested (1) whether predation by crabs and fishes affects the recruitment of benthic species and subsequent community structure and (2) whether the effects of predation vary along the steep gradients of tem- perature, oxygen, sulfide, and metal concentrations near vents. Recruitment substrates (ba- salt cubic blocks, roughly 10 cm on a side), both uncaged and caged to exclude predators (crabs, fishes, whelks, and octopi), were deployed along a decreasing vent fluid-flux gra- dient. The exclusion of predators for 8 mo increased the abundance of small mobile gas- tropods and amphipod crustaceans but decreased the abundance of sessile invertebrates, including juvenile vestimentiferan worms, tubiculous polychaetes, and mussels. Effects of predation were strongest nearest to hydrothermal vents, where abiotic environmental con- ditions were most extreme but productivity and the overall abundances of benthic inver- tebrates and mobile predators were the greatest. Additional 5-mo experiments conducted at three different locations showed similar trends at all sites, indicating that these effects of predation on benthic community structure are repeatable. Stomach-content analyses of the most abundant predators found at vents indicated that the zoarcid fish ( Thermarces cerberus) primarily feeds on the vent snail Cyathermia naticoides, the limpet Lepetodrilus elevatus, and the amphipod crustacean Ventiella sulfuris, the very species that showed the greatest increase following predator exclusion. In contrast, brachyuran ( Bythograea ther- mydron) and galatheid (Munidopsis subsquamosa ) crab stomachs did not contain small mobile grazers, and crabs presented with arrays of the most common vent invertebrate species preferred mussels and vestimentiferans over limpets. Our results indicate that pre- dation by large mobile predators influences the structure of hydrothermal vent communities, directly by reducing the abundance of gastropod prey species, and indirectly by reducing

SUCCESSIONAL MECHANISM VARIES ALONG A GRADIENT IN HYDROTHERMAL FLUID FLUX AT DEEP‐SEA VENTS

Invertebrate communities inhabiting deep-sea hydrothermal vents undergo substantial succession on time scales of months. Manipulative field experiments assessed the relative roles of environmental state and biotic interactions in determining temporal succession along a spatial gradient in vent fluid flux at three vent sites near 9 8509 N on the East Pacific Rise (2500 m water depth). Species colonization patterns on cubic basalt blocks (10 cm on a side) deployed by the submersible Alvin revealed both positive (facilitation) and negative (inhibition) biological interactions, in the context of established succession theory. Over a series of four cruises from 1994 to 1998, blocks were exposed to colonists for consecutive and continuous intervals in short-term (5 1 8 5 13 mo) and longer-term (8 1 29 5 37 mo) experiments. Colonists grouped into a mobile functional group were less abundant in the continuous interval (13 mo) than in the synchronous pooled-consecutive intervals (5 1 8 mo) of the short-term experiment, indicating that early colonists inhibited subsequent recruitment. Colonists grouped into a sessile functional group exhibited the opposite pattern, indicating facilitation. Similar trends, though not statistically significant, were observed in the longer-term experiment. The character of species interactions varied along a gradient in hydrothermal fluid flux (and inferred productivity), with inhibitory interactions more prominent in zones with high temperatures, productivity, and faunal densities, and facilitative interactions appearing where temperatures, productivity, and den- sities were low. Analyses of primary succession on introduced basalt blocks suggest that biological interactions during early vent community development strongly modify initial patterns of settlement, even in the absence of sustained temporal change in the vent fluid flux.

A test of the larval retention hypothesis in seamount-generated flows

Abstract Distributions of larvai of benthic invertebrates in water column near Feiberling Guyot, a talls eamount in the eastern tropical Pacific, were compared with studies of physical oceanographic processes in an effort to test the hypothesis that larvae are retained in seamount-generated flows. Field measurements of currents during 1990 and 1991 had shown that flows near the seamount were driven by tidal rectification, resulting in anticyclonic circulation over the summit and a vertical-radial circulation cell characterized by downwelling at the seamount center, outwelling at the level of the rim, and inward return flows above the level of the rim. No persistent, bottom-trapped, stagnant region was detected on the seamount, but the tidally rectified vertical-radial circulation could theoretically retain larvae. Larval abundances quantified in net samples collected near the seamount in September of 1989 and 1990 were slightly higher near the seamount center than over the flank or base (far field), but did not show the distinct, bottom-trapped aggregation expected from retention in a classic Taylor cap. Larval abundance patterns over the broad region of the seamount (even at the far field sampling locations) were, however, consistent with retention in the tidally rectified circulation. Hydroid colonization on settlement plates suspended on moorings for 6- and 13-month periods (an indirect measure of hydroid larval abundance) was concentrated over a narrow depth range (450–650 m) but extended radially over 40 km away from the seamount center, a pattern also consistent with larval transport and retention in the tidally-rectified circulation cell.

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°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.

Habitat Associations in Gastropod Species at East Pacific Rise Hydrothermal Vents (9°50'N)

At deep-sea hydrothermal vents on the East Pacific Rise (9°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 °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.

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.

Photographic identification guide to larvae at hydrothermal vents

Funding provided by NSF grants OCE-9619605, OCE-9712233, OCE-0424593 and ATM-0428122 and ChEss Grant #WHOI 1334800.

International study of larval dispersal and population connectivity at hydrothermal vents in the U.S. Marianas Trench Marine National Monument

Deep-sea, chemosynthesis-based ecosystems, such as hydrothermal vents, have received increasing attention in the past decade for protection of biodiversity and ecosystem function. For these spatially discrete habitats, dispersal of larvae in the plankton, settlement to the seafloor, and recruitment are processes that connect populations of benthic fauna. Knowledge of these processes is vital to understanding the resilience of vent ecosystems to disturbance or removal of sources of propagules. In particular, hydrothermal vents may be impacted by human activities including scientific research, eco-tourism, bioprospecting, and polymetallic sulfide mining. In 2009 the first Marine Protected Area (MPA) for vents in the U.S. EEZ was established as part of the Marianas Trench Marine National Monument (MTMNM). The vents in this region are located along the Mariana back-arc spreading center (BASC) and volcanic arc.