Craig M. Young

Larval dispersal potential of the tubeworm Riftia pachyptila at deep-sea hydrothermal vents

Hydrothermal vents are ephemeral because of frequent volcanic and tectonic activities associated with crust formation. Although the larvae of hydrothermal vent fauna can rapidly colonize new vent sites separated by tens to hundreds of kilometres, the mechanisms by which these larvae disperse and recruit are not understood. Here we integrate physiological, developmental and hydrodynamic data to estimate the dispersal potential of larvae of the giant tubeworm Riftia pachyptila. At in situ temperatures and pressures (2 °C and 250 atm), we estimate that the metabolic lifespan for a larva of R. pachyptila averages 38 days. In the measured flow regime at a fast-spreading ridge axis (9° 50′ N; East Pacific Rise), this lifespan results in potential along-ridge dispersal distances that rarely exceed 100 km. This limited dispersal results not from the physiological performance of the embryos and larvae, but instead from transport limitations imposed by periodic reversals in along-ridge flows and sustained episodes of across-ridge flow. The lifespan presented for these larvae can now be used to predict dispersal under current regimes at other hydrothermal vent sites.

Reproduction and dispersal at vents and cold seeps

Reproductive cycles are determined from samples taken at regular intervals over a period of time related to the assumed periodicity of the breeding cycle. Fiscal, ship time and sampling constraints have made this almost impossible at deep-sea vents and seeps, but there is an accumulating mass of data that cast light on these processes. It is becoming apparent that most reproductive processes are phylogenetically conservative, even in extreme vent and seep habitats. Reproductive patterns of species occurring at vents and seeps are not dissimilar to those of species from the same phyla found in non-chemosynthetic environments. The demographic structure of most vent and seep animals is undescribed and the maximum ages and growth rates are not known. We know little about how the gametogenic cycle is initiated, though there is a growing body of data on the size at first reproduction. Gametogenic biology has been described from seasonal samples for only one organism from vent/seep environments. For other species, the pattern of gametogenesis has been described from serendipitous samples that allow determination of reproductive effort, but such samples reveal little about energy partitioning during the gametogenic process. Some notable adaptations have been described in mature gametes, including modified sperm. Spawning has been observed for a number of species both in situ and in vitro . Knowledge of the larvae of vent/seep organisms has been derived from laboratory fertilizations, from field collections over vent and seep areas and, for molluscs, from protoconch or prodissoconch size and shape. Larval dispersal has been perhaps the most intractable aspect of reproduction. Because the length of larval life is known for only a single seep organism and no vent organism, we cannot infer dispersal distance from a knowledge of current velocities. Modelling has been used to assess the maximum larval distance that allows effective migration between vent sectors. An indirect approach has been to estimate gene flow within, and between, vent sites using DNA sequencing and electrophoretic techniques. Although data are still equivocal, there are indications of considerable mixing among populations within and between vent sectors of the same ridge. Our knowledge of reproductive biology in vent and seep organisms remains fragmentary, but with molecular and biochemical techniques, emerging larval culture techniques, and increased sampling effort, the pieces of the jigsaw will eventually form an overall picture.

Larval ecology of marine invertebrates: A sesquicentennial history

Abstract Although larval ecology has roots as far back as Aristotle, the earliest accurate ideas about larval recruitment, dispersal, and behavior arose about 150 years ago, during the time of J. Vaughn Thompson and Edward Forbes. In this review, the history of larval ecology is traced from the initial discovery of larvae and the early formulation of ideas in the nineteenth century through the development of methodology for addressing hard-to-study field processes in the 1980s. A survey of the literature in major marine biology journals reveals the overall trends in larval research and the temporal changes in the proportion of effort devoted to various kinds of studies. Many recent studies of larval processes resemble seldom-cited studies that were done more than a half century earlier.

Microhabitat-associated variability in survival and growth of subtidal solitary ascidians during the first 21 days after settlement

Newly settled juvenile ascidians were transplanted into shaded and unshaded sites at two subtidal depths to test the hypothesis that photonegative settlement behavior enhances juvenile survival. Silt, filamentous algae and grazing gastropods (Margarites pupillus) were identified as sources of mortality associated primarily with non-cryptic microhabitats. Silt inflicted heavy mortality on all six species tested. Algal overgrowth was important in shallow water, where it increased mortality and depressed growth rates over a 14-d period. Laboratory experiments demonstrated that gastropods can remove juvenile ascidians from the substratum. The sources of post-settlement mortality investigated may help determine distributional patterns of ascidians in the San Juan Islands, Washington, USA, and may also represent selective pressures that maintain negative phototaxis in the behavioral repertoires of ascidian tadpoles.

Reproductive success in large populations: empirical measures and theoretical predictions of fertilization in the sea biscuit Clypeaster rosaceus

For organisms that free-spawn gametes into the environment, sperm limitation can be a major determinant of reproductive success. Previous tests of sperm limitation have been restricted to very small experimental populations. Here we test and then use a fertilization model to explore sperm limitation in large populations. Predictions of the fertilization model are compared with measures of dye diffusion and in situ fertilization of the sea biscuit Clypeaster rosaceus (Linnaeus). The model could not be rejected in either test. Then this model was used to simulate large-scale spawning events in a natural population of C. rosaceus. The results of our simulations indicate that both population size and population density are important to fertilization over a very large range (2 to over 250000 individuals), but we also found an important interaction between population size and density. The importance of high density was great in small populations but negligible in large populations. This result may provide insight into why aggregation during spawning is not universally seen in nature. Overall, results indicate that sperm limitation can both constrain reproductive success and mediate social behaviors in a wide range in population sizes.

Deep-sea ecology: Developmental arrest in vent worm embryos

Temperature is a key factor in controlling the distribution of marine organisms and is particularly important at hydrothermal vents, where steep thermal gradients are present over a scale of centimetres. The thermophilic worm Alvinella pompejana, which is found at the vents of the East Pacific Rise (2,500-m depth), has an unusually broad thermotolerance (20–80 °C) as an adult, but we show here that the temperature range required by the developing embryo is very different from that tolerated by adults. Our results indicate that early embryos may disperse through cold abyssal water in a state of developmental arrest, completing their development only when they encounter water that is warm enough for their growth and survival.

LABORATORY EVIDENCE FOR DELAY OF LARVAL SETTLEMENT IN RESPONSE TO A DOMINANT COMPETITOR

In nature, the marine bryozoan, Bugula pacifica, is consistently the ‘loser’ when competing for space with the compound ascidian, Diplosoma macdonaldi. We provide laboratory evidence to show that Bugula larvae will delay settling in either ‘Diplosoma-conditioned water’ or an alcohol Diplosoma extract. It is reasoned that the delay response is elicited by an inhibitory factor released continually from Diplosoma. This response is reversible, non-pathological, and species specific. The possible ecological significance of larval avoidance behavior in this and other communities is discussed.

Effects of the duration of larval life on postlarval stages of the demosponge Sigmadocia caerulea

Variability in the duration of the free-swimming period of lecithotrophic larvae of the demosponge Sigmadocia caerulea (Hechtel, 1965) was assessed in the laboratory in the absence of metamorphic inducers and inhibitors. The free-swimming period in three clutches of larvae ranged from 8 to 70 h and the cumulative settlement curve was sigmoid, with settlement peaking between 20 and 28 h after release. There were significant differences among clutches in the time to reach 50% settlement. Within each clutch, small percentages of larvae (<25%) were short-lived (settled less than 12 h after release) or long-lived (settling more than 32 h after release). Juveniles originating from short-lived larvae survived better, grew faster and were more regular in shape than those originating from long-lived larvae. In additional laboratory experiments, we examined the consequences of feeding during the early postsettlement period. Size differences between fed and starved juveniles became apparent 5 days after osculum formation, suggesting that the filter-feeding ability does not begin immediately after osculum formation. Our results are consistent with the hypothesis that long-lived larvae bring fewer reserves to the postsettlement period than do short-lived larvae, thereby experiencing nutritional stress prior to the onset of feeding that can reduce the vigor of the juveniles. Although larvae delaying metamorphosis should theoretically be important in colonizing new habitats and increasing gene flow, low postsettlement survival of such individuals may reduce the evolutionary importance of variability in the duration of the larval period.

Seasonal breeding aggregations in low-density populations of the bathyal echinoid Stylocidaris lineata

Reproduction of bathyal cidaroid sea urchins was studied between 1985 and 1991 with the aid of a manned submersible in the northern Bahamas. During May 1988 and February 1990, discrete, single-species aggregations of Stylocidaris lineata containing 2 to 6 individuals were observed between 510 and 640 m depths. Reproductive conditions of isolated and aggregated individuals were determined histologically. In February, all individuals, regardless of their spatial distribution, contained developing gametes. During the May spawning season, most isolated individuals contained spent gonads with only relict gametes, whereas individuals in discrete aggregations mostly contained ripe gonads with mature or nearly-mature gametes. Aggregations were not observed during the autumn months, when gonads were spent or immature. These data suggest that bathyal cidaroids aggregate for reproduction. An in situ survey during May indicated that pairs of S. lineata are more common than larger clumps, but no more so than predicted by chance. Homosexual and heterosexual pairs occur at the relative frequencies predicted on the basis of sex ratio. We evaluated the need for reproductive aggregation by applying Dennys (1988) model that predicts downstream sperm concentration in a turbulent boundary layer. Flow parameters were measured with dye injected from the submersible, sperm-release rate was estimated in the laboratory, and the relationship between fertilization success and sperm concentration was determined in a laboratory dilution-experiment. The model predicted that, on smooth sandy bottoms at bathyal depths, sperm concentration should remain high enough to fertilize at least some eggs several meters directly downstream from a spawning male. Aggregation may facilitate spawning synchrony, increase gamete encounter probabilities, or cause gametes to be retained at high concentrations near the adults long enough for fertilization to occur.

Factors controlling spatial distribution of the sea cucumber Psolus chitonoides: Settling and post-settling behavior

Substratum selection experiments were carried out in situ with larvae of the holothurian Psolus chitonoides Clark in the rocky subtidal of the San Juan Islands, Washington. The experiments indicated, in agreement with laboratory findings, that pentactula larvae settle gregariously, either on the adult, or (when the bivium is obscured by epizooites) by clustering around the margin of the adult sole. Late larvae and early juveniles are strongly photonegative. Following metamorphosis, juveniles migrate from the adults into nearby shaded habitats, where they may take up residence indefinitely. Although adults retain the capacity to move, they relocate only when their living conditions become unsuitable; in most circumstances they are effectively sessile. Small-scale spatial pattern of the adults, which was documented quantitatively on subtidal rock walls, boulders and cobbles, correlates well with microtopographical features. The aggregation observed in the field is primarily due to post-settling migration rather than larval substratum choice at settlement.