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FAU Institutional Repository FAU Institutional Repository http://purl.fcla.edu/fau/fauir This paper was submitted by the faculty of FAU’s Harbor Branch Oceanographic Institute. Notice: © 1999 Marine Biological Association of the United Kingdom. This manuscript is an author version with the final publication available and may be cited as: Tyler, P.A., & Young, C. M. (1999). Reproduction and dispersal at vents and cold seeps. Journal of the Marine Biological Association of the United Kingdom, 79(2), 193-208. J. Mar. Biol. Ass. U.K. (1999), 79,193^208 Printed in the United Kingdom REVIEW Reproduction and dispersal at vents and cold seeps P.A. Tyler* and C.M. YoungO *School of Ocean and Earth Science, University of Southampton, SOC, Southampton, SO14 3ZH. ODivision of Marine Science, Harbor Branch Oceanographic Institution, 5600 US 1 N, Fort Pierce, FL 34946, USA 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 phylogeneti- cally 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 ¢rst 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 determi- nation of reproductive e¡ort, but such samples reveal little about energy partitioning during the gametogenic process. Some notable adaptations have been described in mature gametes, including modi- ¢ed 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 ¢eld 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 e¡ective migration between vent sectors. An indirect approach has been to estimate gene £ow 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 e¡ort, the pieces of the jigsaw will eventually form an overall picture. INTRODUCTION have also been described from cold seeps but the domi- nant cold seep taxa, such as vestimentiferans and mussels The discovery of hydrothermal vents along the Gala- from the Louisiana slope (Gulf of Mexico) remained pagos Rift some 20 years ago heralded one of the most undescribed more than ten years after ¢rst being observed expansive phases of research in the deep sea. In the inter- and collected (Gustafson et al., in press). vening period, hydrothermal vents have been discovered Since the initial discovery of chemosynthetic endosym- at a large number of locations along mid-ocean ridges bionts in the vestimentiferan tubeworm Riftia pachyptila and back arc basins (Figure 1). Because the bacteria, and (Cavanaugh et al., 1981), an avalanche of publications their symbiotic hosts, in these environments use chemical have described aspects of physiology for a variety of vent energy rather than sunlight as their primary energy and cold-seep species (see Childress & Fisher, 1992 for source, ecosystems driven by chemosynthesis have become review). At present, the autecology of many species is a focus of intense study (Tunnicli¡e et al., 1998). Subse- being unravelled, the ecology of vent communities is quently, these vent studies were supplemented by the being described (Tunnicli¡e, 1991; Van Dover, 1995; discovery of novel cold-seep faunas that share biological Gebruk et al., 1997; Tunnicli¡e et al.,1998), and the evolu- characteristics with hydrothermal vent faunas but at tionary history and fossil record of vent faunas are being ambient, rather than elevated, temperatures (Sibuet & interpreted (Tunnicli¡e, 1991; Tunnicli¡e & Fowler, 1996; Olu, 1998). Jollivet, 1996; Vrijenhoek, 1997). Life history biology, Studies of any new environment generally fall into however, has proved to be the least tractable of biological three consecutive phases: composition, structure and processes, though widely recognized as being of funda- dynamics (Juniper & Tunnicli¡e, 1997). Although over mental importance to understand the establishment and 500 new species have been described from hydrothermal maintenance of vent and seep populations. Of the 500 vents, many more remain to be described. New species putative species described from vent and seep Journal of the Marine Biological Association of the United Kingdom (1999) 194 P.A.Tyler and C.M.Young Vent reproduction and dispersal Figure 1. Distribution of hydrothermal vents (*) and cold seeps (&) in the world ocean. Solid represents sites for which reproductive data are available. Redrawn from an INTERRIDGE base chart. environments, less than ten have been studied primarily larval development, dispersal, settlement and recruitment for their reproductive biology and we do not know the in vent and seep species. Growth is outwith the scope of complete life cycle of a single species of vent or seep this review but is a signi¢cant variable in the life history organism. The di¤culty of studying life history biology biology of an organism and will be referred to as, and stems from a need to examine temporal processes on when, necessary. We have elected to address reproduction scales of months to years in a three-dimensional environ- by examining aspects of the life cycle within speci¢c taxa. ment several orders of magnitude larger than the repro- This allows direct comparisons among related species. ductive propagule. Traditionally, macro- and mega-faunal organisms are sampled repeatedly over multiple years to determine the GAMETOGENESIS, SPAWNING, temporal variation in the various reproductive processes FERTILIZATION AND LARVAL (Giese & Pearse, 1974). Reproduction at vents and seeps DEVELOPMENT might be eminently tractable if we could assume that all Phylum Annelida: Class Polychaeta vent and seep organisms reproduced asynchronously so that at least some members of the population are repro- Polychaete annelids form a signi¢cant element of the ductive at any one time. However, this assumption is unli- vent fauna at most sites studied. They are less dominant kely, as non-vent deep sea organisms are known to have a at cold seeps, although some species found recently are variety of reproductive strategies including asynchronous new to science (Desbruye© res & Toulmond, 1998) and (continuous), synchronous (seasonal) and opportunistic others await description (C. Fisher, K. Eckelbarger, life histories (Gage & Tyler, 1991). From the limited data personal communication). available at present, it is apparent that the reproductive The dominant polychaete genus in the eastern and patterns of vent and seep organisms have strong phyloge- north-eastern Paci¢c is Paralvinella (Table 1). McHugh netic constraints (Van Dover et al., 1985), and that adap- (1989) has compared the reproductive biology of tations to vents and seeps are mainly in the nutritional P. pandorae and P. palmiformis from the Juan de Fuca Ridge and respiratory physiology of the organism. Although the (JdF). Sex ratios are even and gametogenesis is coelomic. general reproductive pattern may be conservative in vent The main gametogenic di¡erences between the two organisms, aspects of the life history must have evolved to species are the smaller egg size and lower fecundity in ensure that the reproductive propagule can ultimately P. pandorae. In addition, the spermatozoon of P. pandorae is locate and colonize the vent `needle' in the oceanic modi¢ed so that the tailpiece recurves at an acute angle `haystack'. from the mid-piece (McHugh, 1995). The modi¢ed sperm In this review the current state of knowledge of P. pandorae suggests that the spermatozoon has limited pertaining to the life histories of vent and seep organisms mobility and spermatozoa are transferred in bundles to are addressed. Our template is the generalized marine the female. Evidence from both the adult population invertebrate life cycle (Figure 2), which includes the structure and oocyte size/frequency data suggest that processes of gametogenesis, spawning and/or copulation, periodicity of reproduction is asynchronous in P. pandorae Journal of the Marine Biological Association of the United Kingdom (1999) Vent reproduction and dispersal P.A.Tyler and C.M.Young
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