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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 195

Figure 2. Marine invertebrate life history pattern. Stages are in bold and the questions posed for each stage are in italics.

Table 1. Known reproductive variables in the polychaete genus Paralvinella.

Paralvinella pandorae1,2 Paralvinella palmiformis1 Paralvinella grasslei3 Paralvinella sul¢ncola4

Site JdF JdF 138N JdF Sex ratio 1:1 ? 1:1 1:1 Gametogenesis Coelomic Coelomic Coelomic Coelomic Oocyte size mm 215 260 275 250 Sperm Modi¢ed Abnormal Abnormal ? Fecundity 4500 18,000 4000 ? Periodicity ?Continuous Periodic Periodic Continuous Spawning/copulation Transfer ? Pseudo-copulation ? Larvae/brooding ?Brood Lecithotrophic/Demersal Benthic Lecithotrophic/Demersal Dispersal distance ? ? ? ? Post-larvae ? ? ? ? Recruitment ?Discontinuous ?Discontinuous Discontinuous ?

Based on 1, McHugh (1989); 2, McHugh (1995); 3, Zal et al. (1995); 4, Jon Copley (1998). JdF, Juan de Fuca Ridge.

Table 2. Known reproductive variables in other genera of Polychaeta.

Alvinella pompejana1,2,3 Amphisamytha galapagensis4 Branchipolynoe seepensis5,6 Hesiocaeca methanicola6

Site EPR JdF Lucky Strike Gulf of Mexico Sex ratio 1:1 1:1 Male biased ? Gametogenesis Coelomic Coelomic Gonad Gonad Oocyte size mm 200 240 400 80 Sperm Abnormal Normal ? Normal Fecundity 2Â104 to 2Â105 ? ? ? Periodicity Periodic Cont/discontinuous Continuous ? Spawning/copulation Internal ? ? External Larvae/brooding Benthic Lecithotrophic ? Trochophore Dispersal distance ? ? ? ? Post-larvae ? ? ? ? Recruitment ? ? ? ?

Based on 1, Jouin-Toulmond et al., 1997; 2,Chevaldonne¨ et al., 1997; 3, Jollivet et al., 1998; 4, McHugh & Tunnicli¡e, 1994; 5,Van Dover et al., personal communication. 6, unpublished observations (D. Jollivet, C.M.Young or P.A.Tyler).

Journal of the Marine Biological Association of the United Kingdom (1999) 196 P.A.Tyler and C.M.Young Vent reproduction and dispersal

Figure 3. Oogenesis in representative invertebrates from hydrothermal vents and cold seeps. (A) Branchipolynoe seepensis from mussels at Lucky Strike. (B) Transverse section of the gonad of the vestimentiferan Lamellibrachia sp. from the Gulf of Mexico. (C) Acini of Bathymodiolus thermophilus from the EPR showing a wide range of oocyte sizes indicative of asynchronous development. (D) Transverse section of the gonoducts of Ridgeia pisceae from the Juan de Fuca Ridge showing eggs and sperm in the gonoducts of a single individual. (E) Bathymodiolus childressi. From the Gulf of Mexico, showing oocytes of even size suggesting a periodicity of development. (F) The gonad of the caridean shrimp Rimicaris exoculata from TAG showing previtellogenic oocytes and well developed vitellogenic oocytes. v, vitellogenic oocytes; e, early vitellogenic oocytes; p, previtello- genic oocytes; o, oocytes; s, mantle tissue; sp, spermatozoa; d, digestive gland. Scale bars: A & D, 100 mm; B, C & E, 50 mm, F, 500 mm. and discontinuous and synchronous in P. palmiformis, thickening may represent an axoneme. On the basis of in though of unknown periodicity. From these data McHugh situ observations, a specialized copulatory behaviour is (1989) hypothesized that P. pandorae has internal fertiliza- suspected (Chevaldonne¨ & Jollivet, 1993). Gametogenic tion and broods its embryos whereas P. palmiformis free- activity is synchronous but of unknown periodicity. spawns its gametes and has a lecithotrophic demersal Larval development seems to be benthic, suggesting larva. limited dispersal. Paralvinella sul¢ncola from the JdF ridge has an oocyte Also found along the EPR is Alvinella pompejana (Table size close to that of P. pandorae (Table 1), but from the 2). This species is sexually dimorphic and produces, in the limited data available there is no evidence of reproductive coelom, between 20,000 and 2Â105 eggs 200 mm in synchrony (Copley, 1998). Paralvinella grasslei, from 138N maximum diameter. Spermatozoa are small, with conical on the East Paci¢c Rise (EPR), demonstrates a di¡erent heads, no mid-piece and a short £agellum (Jouin- reproductive pattern from that of its north-east Paci¢c Toulmond et al., 1997). Gamete production is synchronous congeners (Table 1). The adults are sexually dimorphic and fertilization is internal by pseudocopulation. The (Zal et al., 1994). Gametes develop in the coelom, oocytes larva is believed to be benthic whereas gene £ow is reach 275 mm diameter and fecundity is low (Zal et al., maintained along the EPR (Jollivet et al., 1998; 1995). The spermatozoon is highly modi¢ed (Zal et al., D. Desbruye© res, personal communication). 1994), having no acrosome, £agellum or mid-piece, whilst Reproductive data on other polychaete species are very possessing a £at caudal process in which a longitudinal limited. In Amphisamytha galapagensis from the JdF Ridge,

Journal of the Marine Biological Association of the United Kingdom (1999) Vent reproduction and dispersal P.A.Tyler and C.M.Young 197

Table 3. Known reproductive variables in Vestimentifera.

Riftia pachyptila1 Ridgeia piscesae2,3,5 Lamellibrachia sp.4 Escarpia sp.4

Site EPR JdF GoM GoM Sex ratio ? 1:1 1:1 1:1 Gametogenesis Trunk Trunk Trunk Trunk Oocyte size mm 80/105 85/116 105 115 Sperm Bundles Bundles Bundles Bundles Fecundity High High High High Periodicity No No No No Spawning/copulation External Internal External External Larvae/brooding Trochophore ? Lecithotrophic Lecithotrophic Dispersal distance ? ? ? ? Post-larvae ? Known ? ? Recruitment Natural On tubes ? ?

Based on 1, Cary et al. (1989); 2, Southward & Coates (1989); 3, Goodson et al. (unpublished data); 4, Young et al. (1996); 5, Malakhov et al. (1996); C.M. Young, P.A. Tyler, A. Marsh and D. Manahan, personal observations. EPR, East Paci¢c Rise; JdF, Juan de Fuca Ridge; GoM, Gulf of Mexico. gametogenic development shows no remarkable traits with the ovaries being on the ventral side of the coelom, (McHugh & Tunnicli¡e, 1994) and larval development is and normal sperm. Oogonia develop close to the blood interpreted as lecithotrophic (Table 2). sinuses and each retains a connection to the blood sinus A polynoid worm, genus Branchipolynoe, lives commen- during vitellogenesis (Ramirez et al., unpublished data). sally with both vent and seep mussels. In the Branchipolynoe Gametes are broadcast and the fertilized eggs develop into cf. seepensis from the Lucky Strike vent on the Mid-Atlantic a typical trochophore (C.M.Young, personal observation). Ridge there is sexual dimorphism. There is also a male sex An undescribed orbinid polychaete associated with the bias. In contrast to other vent polychaetes, gametes develop seep mytilids at the Brine Pool on the Louisiana slope has a in well-organized gonads in segments 7 to 9. Egg size is peculiar sperm morphology of unknown function large (500 mm) and these eggs are found in well-developed (K.J. Eckelbarger, personal communication). ovaries (Figure 3A). Fecundity is low (100^200 mature eggs ind71). Fertilization is achieved by copulation and larval development is lecithotrophic (Table 2) (C.L.Van Dover et Phylum Annelida: theVestimentifera al., personal communication; D. Jollivet et al., personal The Vestimentifera form some of the most dramatic communication). images at both hydrothermal vent and cold seep environ- Little is known of the reproductive biology of polychaetes ments. Adult worms in this class are characterized by a from cold seeps. Branchipolynoe seepensis is found associated quasi lack of segmentation and setae, the presence of a with mussels at the base of the Florida escarpment but not vestimentum and obturaculum externally and by the with mussels at bathyal depths on the Louisiana slope. In absence of a functional alimentary system internally. The 1997 Hesiocaeca methanicola Desbruye© res & Toulmond, 1998 trunk region of the adult contains the trophosome, was discovered associated with gas hydrates (solid derived from the alimentary canal, that harbours methane) at site GC232 on the Louisiana slope. This `ice symbiotic bacteria responsible for chemosynthesis. worm' has a gametogenic pattern similar to that described Although species of Vestimentifera vary widely in size, for the hesionid Kerfesteinia cirrata (Olive & Pillai, 1983), and may be found in widely separated geographic

Table 4. Reproductive variables in vesicomyid and solemyid bivalves.

Calyptogena Calyptogena Calyptogena Calyptogena Calyyptogena Calyptogena Acharax magni¢ca1 kilmeri2 paci¢ca2 soyae3 lauberi4 phaseoliformis4 alinae5

Site EPR Monterey Monterey Japan Tenryu Japan Trench Lau Basin Canyon Sex ratio 1:1 ? ? ? ? ? ? Gametogenesis Gonad Gonad Gonad Gonad Gonad Gonad Gonad Oocyte size mm 160/309 180/220 180/220 ? 200 200 660 Fecundity High High High ? Periodicity Asynchronous Seasonal All asynchronous Spawning/copulation All believed to spawn freely Larvae All Lecithotrophic Dispersal ? ? ? ? ? ? `Long range' Recruitment ? ? ? ? ? ? ?

Data from 1, Berg, 1985; 2, Lisin et al., 1996; 3, Endow & Ohta, 1980; 4, Fiala-Medioni & Le Pennec, 1989; 5, Beninger & Le Pennec, 1997. EPR, East Paci¢c Rise.

Journal of the Marine Biological Association of the United Kingdom (1999) 198 P.A.Tyler and C.M.Young Vent reproduction and dispersal

Table 5. Known reproductive variables in mytilid bivalves.

Bathymodiolus Bathymodiolus Bathymodiolus Bathymodiolus Bathymodiolus thermophilus1,2 puteoserpentis3 nov. sp.4 elongatus3 childressi

Site EPR Snake Pit Lucky Strike Fiji GoM Sexuality Dioecious Dioecious Dioecious Protandry Dioecious Sex ratio Male-dominated ? ? ? 1:1 Gametogenesis Mantle Mantle Mantle Mantle Mantle Oocyte size mm 50+ 50 to 60 50 50 to 60 55/90 Fecundity All apparently high but not quanti¢ed Periodicity Asynchronous ?synchronous Highly synchronous Asynchronous ?Synchronous Spawning/copulation All believed to spawn freely Larvae Plankotrophic Planktotrophic Planktotrophic Planktotrophic Planktotrophic Dispersal High ? ? ? Recruitment: Continuous ? Periodic ? Periodic

1, Berg, 1985; 2, Hessler et al., 1988; 3, Le Pennec & Beninger, 1997; 4, Comtet & Desbruye© res,1998; 5, M. Baker, personal communication; :, based on population histograms. EPR, East Paci¢c Rise; GoM, Gulf of Mexico. regions, the reproductive biology of this taxon is very including a lecithotrophic trochophore stage in which conservative (Table 3). The reproductive anatomy of locomotion is accomplished by means of an equatorial species of the cold seep genus Lamellibrachia has been ciliary band (Young et al., 1996) and a more elongate described in detail by Webb (1977) and by van der Land larval form which may have several ciliary bands (C.M. & NÖrrevang (1977), whilst that of Ridgeia piscesae (as Young et al., unpublished data). Gardiner & Jones (1994) R. phaeophiale) are outlined by Malakhov et al. (1996). depict a recently settled juvenile of Ridgeia piscesae that In all vestimentiferan species, gametogenesis takes resembles the elongate, late-stage larva of Lamellibrachia place in gonads that are surrounded by lobes of the sp. (C.M. Young, personal observation). Southward (1988) trophosome. Sexes are separate and eggs are released into and Jones & Gardiner (1988) showed that the youngest the oviduct, in which they pass anteriorly to paired gono- juveniles of R. piscesae have an apparently functional gut, pores on the vestimentum. Although di¤cult to quantify, though it is not known whether larvae become plankto- fecundity is high (Figure 3B) in all species and there is no trophic during the latter part of their planktonic period. evidence of periodicity in reproductive output. Reproduc- tive e¡ort is variable (M. Goodson et al., unpublished data) and it is possible that reproductive e¡ort accounts, Phylum Mollusca in part, for the variable growth rates observed in both Vesicomyid and mytilid bivalves often dominate the vent and cold seep vestimentiferans. The formation of molluscan faunas at vents and cold seeps. Although a sperm is a complicated process (Gardiner & Jones, 1985, number have been described, many more await descrip- 1993; Jones & Gardiner, 1985) with the sperm being tion and the use of molecular techniques has made the transferred, in bundles, along the sperm duct to the vesti- identi¢cations based on adult morphology doubtful mentum. The sperm bundles of Lamellibrachia from Bush (Vrijenhoek et al., 1994; Kojima et al., 1995; Peek et al., Hill on the Louisiana slope disaggregate on contact with 1997). Again we see a remarkable phylogenetic constraint seawater (Young et al., 1996). In situ spawning has been on reproductive processes and early life history stages observed in both Riftia pachyptila (Van Dover, 1994) and (Tables 4 & 5). in Lamellibrachia and Escarpia from the Louisiana slope The only reproductive study to date that has examined (C.M. Young & P.A. Tyler, personal observation). In gametogensis at di¡erent times of the year is that of the cold contrast, Southward & Coates (1989) have described the seep clam Calyptogena kilmeri from the Monterey Canyon sperm of Ridgeia piscesae as being aggregated in masses (Lisin et al., 1997). As in all vesicomyids, gametogenesis is and suggest that internal fertilization occurs in this intragonadal. Fecundity of all species examined appears species. In support of this, Goodson et al. (personal obser- high but has not been quanti¢ed. In C. kilmeri, the vations) provide evidence of both sperm and oocytes proportion of the gonad that is reproductively active within the gonoduct of a single individual (Figure 3D). varies with seasonal but the mean oocyte size does not Sperm have also been observed in the female genital tract (Lisin et al., 1997). Oocytes of all species are 220 mm of Riftia pachyptila (Gardiner & Jones, 1985). in maximum diameter, a size indicative of lecithotrophic Embryonic and larval development have been development (Table 4). There was no indication of repro- described in a preliminary fashion for Lamellibrachia sp. ductive seasonality in the sympatric C. paci¢ca, though and Escarpia sp. from seeps on the Louisiana slope (Young sampling of this species was not as extensive. This is et al., 1996). Early cleavage follows a typical spiralian also the case for C. soyoae from Japan and the vent pattern, with polar lobe formation prior to ¢rst and species C. magni¢ca from the EPR. All species of second cleavages resulting in macromeres of unequal size. Calyptogena examined appear to spawn freely into the Eggs and early embryos are buoyant, but ciliated larvae water column. Fugiwara et al. (1998) have shown, with with the ability to swim eventually lose their inherent in situ experimentation, that the cold seep clam C. soyoae buoyancy. Larvae pass through several distinctive stages, spawns in response to a 0.1 to 0.28C temperature rise.

Journal of the Marine Biological Association of the United Kingdom (1999) Vent reproduction and dispersal P.A.Tyler and C.M.Young 199

Table 6. Known reproductive variables in caridean shrimp and other Crustacea.

Rimicaris Chorocaris Mirocaris Alvinocaris Alvinocaris Munidopsis Munidopsis Bythograea exoculata1 chacei1 fortunata1 lusca1 stactolitha1 lentigo2 subsquamosa2 thermidron2

Site MAR MAR MAR Gal. GoM 218N EPR, Gal. 13, 218N, Gal. Egg size 320 mm 283 mm 350 mm 340 Â500 mm ? 2.2 mm 2.1 mm 480Â540 mm Fecundity 836 ? 361 407 ? 13 294 33,550 Periodicity Evidence of oocyte cohorts in gonad ? ? ? ? ? Spawning/ All presumed to copulate but not observed copulation Larvae Plank. Plank. Plank. Plank. Plank. Lec. Lec. Plank. Dispersal ? ? ? ? ? ? ? ?

1, Based on unpublished data of E. Ramirez and P.ATyler; 2,Van Dover et al.1985. Plank.: Planktotrophic; Lec.: Lecithotrophic. MAR, Mid-Atlantic Ridge; Gal., Galapagos; GoM, Gulf of Mexico.

The males spawn ¢rst and are followed some 20 min press) from the Louisiana slope (M. Baker, P. Tyler & later by the females, though there are occasions when C. Young, unpublished data). Heavy natural recruitment the females fail to spawn. The cause of temperature has been observed in a number of Bathymodiolus popula- rises of this magnitude at cold seeps is unknown. tions (Comtet, 1998; Comtet & Desbruye© res, 1998; Protobranch bivalves are common in deep sea sedimen- C. Young & P. Tyler, personal observation). At Menez tary communities but are rare at vents. The solemyid Gwen and Lucky Strike there is a synchronization of Acharax alinae in soft sediments peripheral to vents in the recruitment periodicity in August and September Lau Basin. Beninger & Le Pennec (1997) have examined (Comtet & Desbruye© res, 1998). two individuals of this species. Oocytes are up to 660 mm Gastropods show the greatest gametogenic variation, diameter and all sizes are present at the same time. The with the majority of species producing a small number of spermatozoa are enormous, with a head and mid-piece large eggs and a few species producing large numbers of 28 mm long and a tail up to 100 mm. These are consider- small eggs (Gustafson & Lutz, 1994). Sperm structure in ably longer than sperm of protobranchs from deep sea vent gastropods has been described by Healy (1990a,b, sediments (Tyler et al., 1993). Beninger & Le Pennec 1992) whilst Hodgson et al. (1997) described the ultra- (1997) propose, on the basis of oocyte size, pelagic structure of spermatogenesis in Lepetodrilus fucensis from lecithotrophic development, or possibly benthic develop- the Juan de Fuca Ridge. Fertilization in this species ment. occurs in the mantle cavity rather than being internal Species of the mytilid genus Bathymodiolus are the most (Fretter, 1988; Hodgson et al., 1997). Gametogenesis, at widespread and abundant of vent and cold seep organ- the ultrastructural level, has been described for isms (with a notable absence at the Juan de Fuca Ridge Bathynerita naticoides, a gastropod abundant at seeps in the and 218N EPR). If all the species described to date Gulf of Mexico (Eckelbarger & Young, 1997; Hodgson et remain within this genus then there is more reproductive al., 1998). Many gastropod species have internal fertiliza- diversity than in other vent and seep genera. Examina- tion and lay encapsulated eggs (Ware© n & Bouchet, 1993). tion of the sexuality of species of Bathymodiolus (Table 5) The aplacophoran Helicoradomenia juani is hermaphroditic, suggests that B. thermophilus from the Galapagos vents, as is normal for neomenioid aplacophorans, and produces B. elongatus from the Fiji Basin and Bathymodiolus sp. nov. eggs of 80 mm diameter. from Lucky Strike on the Mid-Atlantic Ridge (MAR) are hermaphrodites (Berg, 1985; Le Pennec & Beninger; 1997, Comtet, 1998). Bathymodiolus thermophilus from the Phylum Crustacea: Order Decapoda EPR, B. puteoserpentis from Snake Pit on the MAR and In contrast to the Paci¢c vents, Atlantic vents are B. childressi from the Louisiana slope are dioecious dominated by caridean shrimp or by mytilids. Although (Table 5) (Le Pennec & Beninger, 1997; M. Baker, less taxonomic uncertainty surrounds the identi¢cation of personal communication). species within this taxon, there has been some confusion Except for di¡erences in their conditions of sexuality, with both the suppression and erection of genera species of vent and seep mytilid appear to have similar (Vereschaka, 1996). In addition to the shrimp that domi- reproductive variables. Gametogenesis is mytilid-like; it nate the deeper vents in the Atlantic (Table 6), species of starts in a posterior gonad and progresses throughout the the genus Alvinocaris are found at vents and cold seeps in mantle. Oocyte size is 50 mm (Figure 3C & E) and both the Paci¢c and Atlantic. fecundity is high, which together with evidence of Examination of the pre-spawning reproductive prodissoconch size is suggestive of a planktotrophic larva processes suggests a marked conservatism in caridean (Lutz et al., 1980; Le Pennec, 1988; Le Pennec & shrimp reproduction. In general, egg size is about 300 to Beninger, 1997; P.A. Tyler, personal observation). 400 mm and the oocytes are produced in cohorts within Periodicity of reproduction is di¤cult to determine from the ovaries (Figure 3F). Fecundity is variable but rela- limited samples but there is evidence of a sexual pause in tively low (between 836 eggs/female in Rimicaris exoculata B. puteoserpentis, and Bathymodiolus n. sp. from Lucky and 5400 in Mirocaris (formerly Chorocaris fortunata). Strike, MAR (Comtet, 1998) and periodicity of gameto- Intra-speci¢c variation may be a function of adult size. genesis in Bathymodiolus childressi (Gustafson et al., in Although eggs are released as cohorts onto the pleopods,

Journal of the Marine Biological Association of the United Kingdom (1999) 200 P.A.Tyler and C.M.Young Vent reproduction and dispersal

Table 7. Measured and inferred £ow close to Mid-Oceanic Cary & Giovanni (1993) have demonstrated, by Ridges (values in cm s71). molecular techniques, the transovarial inheritance of endosymbionts in C. magni¢ca, C. phaseoliformis and Site Flow C. paci¢ca. Evidence is still lacking for transovarial inheritance in the genus Bathymodiolus (Le Pennec & Juan de Fuca 5 to 20 Beninger, 1997). In Riftia, although there has been much East Paci¢c Rise `Few' searching, there is lack of evidence for transovarial inheri- 108N 1 to 2 (mean maximum) tance, the current suggestion being that the juvenile 138N 4.2 to 5.2 vestimentiferan obtains bacteria from free living popula- Axial Seamount 4 tions on settlement (horizontal transmission) (Southward, Mid-Atlantic Ridge 20 (variable) 1988; Cary et al., 1989; Cary & Giovanni, 1993). This is Data from Cannon et al. (1991); Cannon & Pashinski (1990); supported by recent work with Lamellibrachia larvae (S.C. Mullineaux & France (1995); Chevaldonne¨ et al. (1997); Kelvin Cary & A. Pile, unpublished data). Richards, personal communication. DISPERSAL there is no obvious synchrony across the population. All Many workers have speculated about the mechanisms species are believed to copulate and there is evidence by which new vents are colonized and by which popula- from video recording that this takes place in the water tions are maintained at existing vents, because vent habi- around vents (D. Desbruye© res, personal communication). tats are often ephemeral and vent organisms have highly Larval development is planktonic (D. Dixon, personal specialized habitat requirements. Seep habitats tend to be communication). In M. fortunata from the shallower temporally more stable, but specialized needs of the resi- Atlantic vents, berried females are not uncommon dent species should nevertheless require either mechan- (D. Dixon & P.A. Tyler, personal observation) but isms for retaining larvae or for dispersing at scales berried females of R. exoculata are very rare. Considering appropriate for locating new seeps. the large numbers of R. exoculata that have been collected The currents that advect and disperse larvae have been from the deep Atlantic vents, the total number of berried measured at several vents and seeps (Table 7). Flow is females found is less than 20. It is possible that berried often low but may be variable and is often turbulent. The adults move away from the vent to protect the developing position of the larvae in the water column is signi¢cant, embryos, although it is also possible that eggs are released as £ow direction and speed varies with height above the into the plume before hatching (A. Vereschaka, personal bottom. communication), as plankton samples from the plume of Dispersal ability may be inferred from: (1), length of Broken Spur had eggs forming 95% of the biomass. larval life and the speed and direction of ambient Squat lobsters and crabs form an important element of currents; (2), direct collections of planktonic larvae; (3), the higher levels in the food chain of vents. At seeps crabs studies of respiration; and (4), studies of genetic similarity appear to be absent. In general, their reproduction has between disjunct populations. The depths at which larvae received little attention (Table 6). Fecundity in Munidopsis disperse may be inferred from biochemical markers, and lentigo and M. subsquamosa is low and their large egg size is from studies of physiological tolerances. indicative of lecithotrophic development (Van Dover et al., 1985). By contrast, Bythograea thermidron produces large numbers of small eggs, indicative of planktotrophic devel- Dispersal inferred from the culture and collection of larvae opment. Megalopae are frequently found in sediment Although larval culture is a common practice in traps moored near vents (D. Desbruye© res, personal studies of shallow water marine invertebrates, the in vitro communication). culture of larvae from deepwater vents and seeps has proved challenging. To date, from the vent and cold seep Other taxa dominants, only the larvae of the Louisiana slope vesti- mentiferans Lamellibrachia and Escarpia have been raised Very little is known of the reproductive biology and in the laboratory. Embryos of these species developed into development of other taxa at vents and seeps. The lecithotrophic trochophore-type larva that survived for ophiuroid Ophioctenella acies, which occurs abundantly at 21 days (Young et al., 1996). Current measurements at seeps on the Mid-Atlantic Ridge, has a gametogenic the seeps suggest that larvae should disperse about 40 to pattern similar to that of other ophiurids (P.A.Tyler, 60 km during this period. Of vestimentiferans living at personal observation). the deeper hydrothermal vents, embryos of both Riftia pachyptila has been reared as far as a trochophore under pressure (A. Marsh & D. Manahan, personal communi- TRANSMISSION OF SYMBIONTS cation) and Ridgeia piscesae have been reared as far as the A signi¢cant challenge in understanding reproduction 16-cell stage (V. Tunnicli¡e, personal communication). and dispersal at vents has been to determine how the In the vent shrimp Mirocaris fortunata, from Lucky Strike chemosynthetic bacterial endosymbionts of metazoans are and Menez Gwen venting areas the ¢rst zoeal stage has transferred to subsequent generations. The data to date been obtained from in vitro hatchings at 1 atm. (D. remain equivocal. Endow & Ohta (1990) demonstrated, Dixon, personal communication). by ultrastructure, that the bacterial symbiont of Molluscs have been more tractable than other taxa for Calyptogena soyoae is transferred vertically in the oocyte. inferring the mode of larval development because the

Journal of the Marine Biological Association of the United Kingdom (1999) Vent reproduction and dispersal P.A.Tyler and C.M.Young 201

Table 8. Larval densities at Mid-Oceanic Ridges. In the Atlantic, larval shrimp have been taken in rectangular mid-water trawl (RMT) 1+8 nets towed Site Density (ind1000 m73) both in the proximity of vents and at a distance from vents (P. J. Herring & D.R. Dixon, 1998). Guaymas Basin 200 Overall, data on the density and distribution of vent 98N EPR 800 and seep larvae are rare (Table 8). Available data suggest Juan de Fuca 90 that density of larvae may be higher over sedimented Juan de Fuca Calyptogena 4 sites, such as the Guaymas basin, than at rocky sites.

Based on Berg & Van Dover, 1987; Wiebe et al., 1988; Mullineaux et al.,1995. Dispersal inferred from gene £ow Early observations of genetic structure between Gala- pagos and EPR suggested that gene £ow may be limited larval shell is preserved at the apex of the adult shell. The (Grassle, 1985), but with increased sampling e¡ort gene size of the larval shell, the ratio of prodissoconch I and II £ow has been shown to be su¤cient to counteract drift in bivalves, and the number of whorls of the protoconch over large spatial scales (Table 9). Divergence among in gastropods, indicates planktotrophic or non- populations is estimated by FST, which under the `Island planktotrophic development (Lutz et al., 1980, 1984; Model' (Wright, 1931) is inversely related to gene £ow,

Lutz, 1988; Gustafson et al., 1991; Gustafson & Lutz, Nm. Nm is the average number of migrants exchanged 1994; Mullineaux et al., 1995, 1996). This method cannot, between sites per generation. It should be greater than however, distinguish between pelagic lecithotrophic one to prevent di¡erentiation through genetic drift development and encapsulated or direct development on (Chevaldonne¨ et al., 1997; Black et al., 1998). Of the the sea £oor. Of the 30 species of vent mollusc examined dominant species, Riftia pachyptila, Bathymodiolus by Lutz et al. (1986), 27 were deemed to have non- thermophilus, Calyptogena magni¢ca and limpets, living along planktotrophic development. Only species of Bathymodiolus the EPR and the Galapagos Rift, all show evidence of were believed to have `long-lived widely-dispersing high gene £ow (Black et al., 1994; Craddock et al., 1995; larvae'. However, various molluscan larvae are readily Jollivet et al., 1995; Karl et al., 1996; Craddock et al., identi¢able in plankton samples to the speci¢c level 1997). However, after rigorous re-analysis of Black's data, (Mullineaux et al., 1995), suggesting that many of the Vrijenhoek (1997) suggests some genetic variation consis- non-planktotrophic forms must in fact disperse away from tent with isolation by distance although such analyses are the parental habitat. At low deep sea temperatures, it a¡ected by the occurrence of the Hess Deep and the cannot necessarily be assumed that lecithotrophic larvae bathymetry between Guaymas and EPR. There is, also are limited in their dispersal capabilities (Young et al., signi¢cant genetic divergence between populations of the 1997). amphipod Ventiella sulfuris living on the EPR and the To quantify larval abundance, it is necessary to sample Galapagos Rift, suggesting an interruption of gene £ow vent surroundings using nets (Berg & Van Dover, 1987; between these two ridge areas, generally attributed to the Wiebe et al., 1988), pumps (L. Mullineaux, personal 5000-m deep, 50-km wide Hess Deep (France et al., communication) or sediment traps (Comtet, 1998). In the 1992). These authors suggest that the high gene £ow most successful study to date, Mullineaux et al. (1995) con¢ned to the EPR is a result of juvenile or adult towed a MOCNESS net both along and across the vent dispersal, as V. sulfuris, being a peracarid, broods its plume at Axial Seamount on the JdF Ridge, while simul- young. taneously measuring the light attenuation anomaly (Dc). In the Atlantic, high levels of gene £ow in the caridean These data demonstrated that larvae of vent gastropods shrimp Rimicaris exoculata between TAG and Broken Spur, and Calyptogena were associated with the plume whilst separated by 380 km, has been estimated by Creasey et non-vent larvae were found only in non-plume seawater. al. (1996). This high gene £ow can also be extended south Kim et al. (1994) modelled larval dispersal in both the to the R. exoculata populations at Snake Pit (Shank et al., plume and near-bottom currents. Along the EPR, they 1998b; R. Vrijenhoek, personal communication). estimated a mean vertical £ux of 100 larvae h71 in a Geomorphological barriers may impede gene £ow. In single black smoker plume, concluding that plumes were the Paci¢c, the Hess Deep impedes gene £ow in V. sulfuris a signi¢cant mechanism for dispersal. Subsequently, Kim whilst the 240 km o¡set of the Riviera Fracture Zone at & Mullineaux (1998) modi¢ed these ideas, suggesting 188N on the EPR may prevent the northward dispersal of that plume-level transport dominates 526% of time, larvae of Bathymodiolus thermophilus (Craddock et al., even in vigorous black smokers, and that 53% of larvae 1995). This same fracture zone, however, does not impede are entrained in plumes. Kim & Mullineaux (1998) gene £ow in other species (Black et al., 1994, 1998; Vrijen- demonstrate that the main transport of larvae is by cross- hoek, 1997). In the north-east Paci¢c gene £ow, in Ridgeia, axis £ows with tidal excursions of up to 2 km. Flows near is impeded at the 360 km o¡set of the Blanco Transform the seabed carried more larvae than those 15 m above the Fault between the JdF and the Gorda Ridges, but not by bed. Although Kim & Mullineaux (1998) believe that the Sovanco Transform Fault between Middle Valley and plume transport dominates only during slow current Southern Explorer Ridge (Southward et al., 1996; Black speeds, they note that larval dispersal in megaplumes et al. 1998). In the Atlantic no barriers to gene £ow other (Baker, 1994) remains unquanti¢ed but may be respon- than depth have been identi¢ed, although Iceland may be sible for the occasional large pulses of larvae found over a major barrier since vents, but not vent fauna, are the JdF Ridge. known north of Iceland (Van Dover, 1995).

Journal of the Marine Biological Association of the United Kingdom (1999) 202 P.A.Tyler and C.M.Young Vent reproduction and dispersal

Table 9. Dispersal of vent organisms as measured by genetic distance within metapopulations.

: Species Location Method Gene £ow/Nm Ref.

Paralvinella grasslei 11, 13, 218N EPR Galapagos, Guaymas Allozyme High/3.4 6, 12 Alvinella pompejana 13, 218N EPR Allozyme High/5.7 6, 12 Alvinella pompejana 138N EPR rDNA RFLP High/5.2 14 Alvinella caudata 13, 218N EPR Allozyme High/6.7 6, 12 Riftia pachyptila Galapagos; 218N EPR Allozyme High 2 Riftia pachyptila 9, 11, 13, 218N EPR, Galapagos, Guaymas Allozyme High/5.4 4, 12 Ridgeia piscesae JdF, Explorer Allozyme High/3.3 9 Gorda DNA High/3.3 13 Tevnia jerichonana 9, 11, 138N EPR Allozyme High/2.4 12, 13 Oasisia alvinae 9, 11, 13, 218N EPR Allozyme Low/1.2 13 Bathymodiolus sp. Lau, Fiji, Allozyme High 5 Bathymodiolus thermophilus 138N, Galapagos Allozyme Low 1 Bathymodiolus thermophilus 9, 11, 138N, Galapagos Allozyme/DNA High/5.5 7 Calyptogena magni¢ca 9, 218N, 188S, Gal Allozyme/DNA High/11.7 10 Lepetodrilus elevatus elevatus 9, 11, 13, 218N EPR, Gal Allozyme Low/1.8 11 Lepetodrilus elevatus galriftensis 9, 13, 218N EPR Allozyme Low/1.4 11 Lepetodrilus pustulosus 9, 11, 138N EPR, Galapagos Allozyme High/2.5 11 Eulepetopsis vitrea 9, 11, 13, 208N EPR, Gal Allozyme Low/1.0 11 Ventiella sulfuris 118N EPR, Galapagos Allozyme High on EPR/0.3 3 Rimicaris exoculata TAG, Broken Spur (MAR) Allozyme High/250 8, 15

Based on 1, Grassle (1985); 2, Bucklin (1988); 3, France et al. (1992); 4, Black et al. (1994); 5, Moraga et al. (1994); 6, Jollivet et al. (1995); 7, Craddock et al. (1995); 8, Creasey et al. (1996); 9, Southward et al. (1996); 10, Karl et al. (1996); 11, Craddock et al. (1997); 12,Vrijenhoek 13 14 : (1997); , Black et al. (1998); , Jollivet et al. (1998); Shank et al. (1998b). For de¢nition of Nm see text. See Figure 1for sites. , High and low are relative terms. N m values approaching1may be di¡erentiation that has occurred just by drift (D. Jollivet, personal communication).

D. Desbruye© res (personal communication) believes that larval culture. Embryos of the seep vestimentiferan hydrological barriers, as yet unquanti¢ed, will prove to Lamellibrachia tolerated all pressures to 200 atm but died be signi¢cant barriers to gene £ow. However, there is at greater pressures (Young et al., 1996). Larvae of this evidence of genetically isolated populations of species are intolerant to temperatures (14 to 168C) found Bathymodiolus spp. at Lucky Strike, Menez Gwen, Broken above 200 m depth (C.M. Young & P.A. Tyler, unpub- Spur, Snake Pit and Logatchev (Comtet, 1998). lished data). Respiration rates measured for Lamellibrachia and compared to energy available in the egg indicate that the larvae should be capable of dispersing for about three Dispersal inferred from lipid biomarkers weeks which is the same range as the observed duration Lipids within an organism can trace the food source used of larval life in laboratory cultures (P. Leong, D. by that organism. Lipid biomarkers have distinct signatures Manahan & C.M. Young, unpublished data). and it is possible to determine whether these originated We have subjected the ¢rst larval stage of Mirocaris from phytoplankton or from chemosynthetic bacteria. fortunata to various pressure/temperature combinations. Larvae and juveniles of vents shrimp, particularly Rimicaris Maximum pressure tolerated was 300 atm that corre- exoculata, have lipids indicative of a phytoplanktonic origin sponds to their occurrence at Broken Spur, the deepest (Rieley et al., 1995; Pond et al., 1997a,b,c; C. Allen, site at which they are found. The larvae were able to personal communication). As the juveniles grow in the vent tolerate 1atm at 108C, but died at 1atm at 208C habitat, phytoplankton-derived lipids are replaced by lipids suggesting that the thermocline may be a signi¢cant of bacterial origin. This suggests an ontogenetic change in barrier to upward dispersal. trophic behaviour with larvae feeding on phytoplankton or organisms that have consumed phytoplankton at some unde¢ned level of the water column. It should be noted, RECRUITMENT however, that phytoplankton cells are abundant on the Recruitment has been observed at newly active vents seabed in the vicinity of Atlantic vents and are resuspended and community succession has been documented (Hessler by currents in the benthic boundary layer (D. Desbruye© res, et al. 1988; Lutz et al., 1994; Jollivet, 1993, 1996; Tunni- personal communication). In Paci¢c adult vent species, the cli¡e et al., 1997; Shank et al. 1998a). Although recruit- level of bacterially-derived lipid biomarkers is very high ment at a new vent has been described from the EPR with an insigni¢cant input from phytoplankton (C. Allen, (Lutz et al., 1994), supply of recruits was deemed to be personal communication). local. Within the ¢rst year white bacterial mats were present, followed by vestimentiferans (initially Tevnia jerichonana at 11 months and Riftia pachyptila by 32 Dispersal inferred from larval tolerances and respiration months). Within 32 months, Riftia pachyptila had attained Larval tolerances are poorly quanti¢ed in vent and reproductive maturity and was spawning (Lutz et al., seep organisms because of the intractability of in vitro 1994; Shank et al., 1998a). By year 5, a fully developed

Journal of the Marine Biological Association of the United Kingdom (1999) Vent reproduction and dispersal P.A.Tyler and C.M.Young 203 community was present. An enigma in this community suggests planktotrophic development, the majority of vent development was the presence of local populations of organisms produce an egg size indicative of lecithotrophic Bathymodiolus thermophilus and Calyptogena magni¢ca but no development, which may take place either in the water recruitment of these two species to the new vent column or on the bottom. Such data should be interpreted (Vrijenhoek, 1997). From the study of a new vent on the with care, as the relatively small egg size (110 mm) in JdF, the nearest source of larvae was at least 18 km vestimentiferans would be considered indicative of plank- distant (Tunnicli¡e et al., 1997). First larval recruits were totrophy in many groups, but larval rearing of vestimentiferans, alvinellid polychaetes and nemerteans. Lamellibrachia sp. from the Gulf of Mexico, shows these Two years after the initiation of venting, 33% of the small eggs develop into lecithotrophic larvae (Young et regional species pool was present at the vent. al., 1996). Experimental recruitment to arti¢cial settlement panels Planktotrophic larvae are generally assumed to has proved more di¤cult.Van Dover et al. (1988) exposed disperse for much longer distances than lecithotrophic panels for 26 d and1216 d. Gastropods recruited within 26 d larvae (Vrijenhoek, 1997), but this generalization is now with populations of post-larval and juvenile polychaetes, being challenged. Shilling & Manahan (1994) have molluscs and barnacles being found on all panels. Recruit- shown that Antarctic lecithotrophs may have a pelagic ment was considered continuous rather than episodic owing existence of up to 60 months whereas in planktotrophs to the population structure observed at 1216 d. Recruitment the maximum larval life was 10 months. In addition, the of serpulid worms was discontinuous to arti¢cal plates over highly productive vent sites are surrounded by oligo- a 3-year period (Jollivet, 1993). Mullineaux et al. (1998) trophic waters, that provide very little nutrition for devel- placed basalt blocks in four separate zones at 9850'N on the oping planktotrophs as they are advected away from EPR: the vestimentiferan, bivalve, suspension feeder and vents. If egg size is phylogenetically constrained, selective peripheral zones. Mussels and serpulid polychaetes colo- pressure at vents may have favoured species with yolky nized zones outside the adult range: mussels into the vesti- eggs that provide su¤cient food reserves for long-distance mentiferan zone and serpulids into both the mussel and dispersal in oligotrophic waters. This paradigm has been vestimentiferan zone. Recruitment by the vestimentiferan recently established for non-vent deep sea organisms Tevnia supported previous observations that this species is (Young et al., 1997). an initial colonist at newly-formed vents along the EPR. Recruitment by Lepetodrilus elevatus suggested that a region- wide synchronous settlement event had occurred not long Spermatogenesis before recovery of the plates. From these data, Mullineaux Although one may expect spermatogenesis to be a very et al. (1998) interpreted that recruitment at vents varied conservative process, there are a number of examples of temporally and that post-settlement interactions were unusual sperm morphology in vent and seep organisms. important in structuring the vent community. The modi¢ed sperm of Alvinella pompejana, Paralvinella pandora and P. grasslei, the formation of sperm bundles in DISCUSSION Vestimentifera, and the evidence for sperm transfer in some vestimentiferans suggests adaptations to ensure The traditional methods for reproductive analysis are successful fertilization in a turbulent or physiologically compromised at vents and seeps because of ¢scal and stressful environment. Many alvinellids, as well as gastro- technical constraints of studying these environments. pods, limpets have a copulatory process to ensure Time-series analyses from the deep sea are rare and have successful fertilization. often been accomplished by sampling over many years and integrating the data from di¡erent years onto a single annual axis (Gage & Tyler, 1991). Because of the di¤culty Initiation and timing of gametogenesis of sampling in the deep sea at large, and at hydrothermal The initiation of gametogenesis is poorly understood in vents and cold seeps in particular, the knowledge we even shallow water species. Evidence from vent species glean has to be extrapolated from a limited number of suggests that reproductive development starts when the samples and by comparison with known established adult has reached a low percentage of its ¢nal size. The patterns. As a result, our knowledge of life histories rate at which individuals mature still waits to be quanti- (Figure 2) remains fragmentary for vent and seep organ- ¢ed, but both Riftia pachyptila and Ridgeia piscesae are able isms, but the pieces of the jigsaw are being emplaced. to reproduce within one or two years of settling at a new Oogenic patterns of vent species are very similar to vent (Lutz et al., 1994; Tunnicli¡e et al., 1997). those of closely-related non-vent species. The main vari- ables in oocytes are the spawning size, the pattern of vitellogenesis (autosynthesis or heterosynthesis of yolk) Synchrony or asynchrony of reproduction and the amount of yolk laid down. As initially suggested Owing to the lack of repetitive or seasonal samples, by Van Dover et al. (1985), and from subsequent observa- gametogenic synchrony has been one of the most tions, the process of oogenesis in hydrothermal vent intractable aspects of understanding the reproductive organisms is very conservative, apparently constrained by biology of vent organisms. From non-vent deep sea the phylogeny of the organism. species, Tyler et al. (1982) demonstrated that species that had synchrony of gamete development within a sample, Signi¢cance of egg size but no synchrony of gamete development between With the notable exception of the massive egg produc- samples, were periodic or synchronous (usually seasonal) tion in Bathymodiolus, whose oocyte size (50 mm) in their gametogenic development. Those that had

Journal of the Marine Biological Association of the United Kingdom (1999) 204 P.A.Tyler and C.M.Young Vent reproduction and dispersal asynchrony of gamete development in a sample but other crustaceans, presumably copulate as do shallow synchronous in the additive between-sample development water crustaceans in general. were `continuous' or asynchronous breeders. It is not surprising that many species ensure successful The only truly seasonal analysis of the gametogenic fertilization by pseudo- or real copulation. In the turbu- pattern in a vent or seep species is that of Calyptogena lent vent environment, sperm will soon be dispersed and kilmeri from the Monterey Canyon seeps (Lisin et al., diluted to a concentration insu¤cient to ensure successful 1997). Oocyte size/frequency did not vary throughout the fertilization. Pennington (1985) has demonstrated that year but the proportion of the gonad undergoing repro- echinoid sperm are diluted rapidly beyond fertilization duction did. Of non-seasonal sampling of vent organisms, densities in turbulent £ow. The dense juxtaposition of oocyte size/frequency and stages of gametogenesis in individuals within a vent or seep population should aid Amphisamytha galapagensis suggest quasi-continuous repro- successful fertilization. It is not uncommon to observe duction. Paralvinella pandorae also appears to have quasi- several individual vestimentiferans spawning within a few continuous gametogenic development, whereas there were seconds of each other in dense aggregations. discrete breeding periods in the congeneric species P. palmiformis and P. grasslei (McHugh, 1989; Zal et al., 1995). The intrageneric variation in reproductive period- Larval development, dispersal, settlement and recruitment icity is re£ected in the bivalve genus Calyptogena, where an An understanding of dispersal and recruitment of apparent seasonal variation was found in C. kilmeri whilst reproductive propagules from and to, current and new continuous reproduction was observed in C. paci¢ca. hydrothermal vents is the holy grail of reproductive Because of the confusion of the systematics of vesicomyids biology at vents and seeps. Dispersal is a function of the (Vrijenhoek et al., 1994) care should be taken in duration of larval life and the direction and magnitude of comparing reproductive characteristics of di¡erent prevailing currents. Recruitment relies on the reproduc- species. Le Pennec & Beninger (1997) report discontin- tive propagule locating and settling at a vent site without uous gametogenesis in Bathymodiolus species from vents at the aid of being able to swim signi¢cantly in any direc- 138N on the EPR, Snake Pit on the MAR and the North tion. The initial observation that the same species was Fiji Basin. In addition, our unpublished work (M. Baker, found at two or more vents (Lutz, 1988) and the subse- P.A. Tyler & C.M. Young, unpublished data) suggests quent genetic studies (for references see Table 9) suggest there is synchrony in the gametogenic development of that the same population inhabit a series of vents often Bathymodiolus childressi from the Louisiana cold seeps. many hundreds, if not thousands, of kilometres apart. Synchrony of recruitment is seen in the settlement of This attested to the dispersal ability of the species and Lepetodrilus elevatus on plates exposed for 36 months at stressed the importance of an understanding of dispersal 98N (Mullineaux et al., 1998). Two episodic recruitments and recruitment to and from isolated islands of hydro- events were identi¢ed but the periodicity of these events thermal activity. could not be determined. Synchrony between populations Larval development in practically all vent and seep has been shown in the recruitment of Paralvinella grasslei non-mollusc invertebrates remains poorly known. In vitro from the EPR and Bathymodiolus nov. sp. from Lucky fertilization and larval rearing have been successful for Strike (Zal et al., 1995; Comtet & Desbruye© res, 1998). the cold seep vestimentiferans Lamellibrachia and Escarpia (Young et al., 1996) and the `ice-worm', Hesiocaeca methanicola, (E. Ramirez, S. Brooke & C.M. Young, Spawning and/or copulation personal observation). Success with the deeper-living vent In situ spawning of hydrothermal and cold seep organ- species has been more limited. Embryos of Riftia have isms has been rarely observed, because free-spawning recently been cultured as far as a trochophore (A. Marsh species do not spawn all the time and the majority of & D. Manahan, personal communication). Larvae of the species at vents do not appear to be free spawners. Van vent crab Bythograea sp. have been maintained successfully Dover (1994) reports the observation of in situ spawning in culture (C. Cary, personal communication). These in Riftia pachyptila on the EPR. We have observed e¡orts will eventually aid in understanding dispersal, Lamellibrachia sp. spawning at cold seeps in the Gulf of once the observations are interpreted in the context of Mexico (C.M. Young & P.A. Tyler, personal observa- measured £ow regimes both near and far from vent tions). By contrast, Southward & Coates (1989) found systems. sperm masses on female Ridgeia and recent observations Dispersal potential of vent organisms has been inferred have found sperm in the gonoduct of a female specimen from the genetic structure of populations, and the poten- of Ridgeia piscesae (Goodson et al., unpublished observa- tial for migration to the upper water column has been tions). Both observations indicate some form of sperm assessed by studies of biochemical markers and physio- transfer. Bathymodiolus childressi has been induced to spawn logical tolerances of larval stages (Pond et al. 1997a,b,c: freely when maintained in Plexiglass boxes on the sea C. Allen, personal communication; P.A. Tyler, personal £oor (D. Vaughan, personal communication). External observation). There is a growing body of evidence to fertilization is reported for Amphisamytha galapagensis suggest that gene £ow may be high along speci¢c ridges (McHugh & Tunnicli¡e, 1994) but this has not been (Vrijenhoek, 1997). The `stepping stone model' (Kimura observed in nature. In Paralvinella pandorae fertilization & Weiss, 1964) predicts a high genetic similarity between takes place either in the tube or in a gelatinous mass adjacent populations which is negatively correlated with outside the tube (McHugh, 1995). All species of alvinel- distance. Such a pattern is seen in the EPR vestimenti- lids appear to have some form of pseudo-copulation to ferans Riftia pachyptila, Tevnia jerichonana and Oasisia alvinae ensure successful fertilization. Caridean shrimp, and (Vrijenhoek, 1997; Black et al., 1998) but not in Ridgeia

Journal of the Marine Biological Association of the United Kingdom (1999) Vent reproduction and dispersal P.A.Tyler and C.M.Young 205 piscesae from the JdF Ridge (Southward et al, 1996). The Berg, C.J.J. & Van Dover, C.L., 1987. Benthopelagic alternate model is the `island model' (Wright, 1931) where zooplankton communities at and near deep-sea hydrothermal all populations contribute to and recruit from a single vents in the eastern Paci¢c Ocean and the Gulf of California. widespread well-mixed larval pool. Bathymodiolus Deep-Sea Research, 34, 379^401. thermophilus and Calyptogena magni¢ca conform to this Black, M.B., Lutz, R.A. & Vrijenhoek, R.C., 1994. Gene £ow among vestimentiferan tube worms (Riftia pachyptila) popula- model. That species with such di¡erent reproductive tions from hydrothermal vents of the eastern Paci¢c. Marine modes (planktotrophic in B. thermophilus, lecithotrophic in Biology, 120, 33^39. C. magni¢ca) conform to this model suggests that the Black, M.B., Trivedi, A., Maas, P.A.Y., Lutz, R.A. & reproductive mode, although phylogenetically constrained, Vrijenhoek, R.C., 1998. Population genetics and biogeo- is well adapted to maintain the population at a vent and graphy of vestimentiferan tubeworms. Deep-Sea Research II, 45, colonize new vents. However, although vestimentiferans 365^382. appear to conform to the stepping stone model, their high Bucklin, A., 1988. Allozyme variability of Riftia pachyptila popu- fecundity, continuous reproduction, successful fertilization lations from the Galapagos Rift and 218N hydrothermal and highly dispersive larval stage, place them among the vents. Deep-Sea Research, 35, 1759^1768. ¢rst organisms to colonize new vent sites (together with Cannon, G.A. & Pashinski, D.J., 1990. Circulation near Axial polychaete worms). Seamount, Juan de Fuca Ridge. Journal of Geophysical Research, 95, 12823^1228. Chevaldonne¨ et al. 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Transovarial inheritance of maximum population size, maximum density and high endosymbiotic bacteria in clams inhabiting deep-sea hydro- fecundity, was determined to be 30 d, which was less than thermal vents and cold seeps. Proceedings of the National Academy of Science, 90, 5695^5699. the time of advection of a parcel of water between two Cavanaugh, C.M., Gardiner, S.L., Jones, M.L., Jannasch, H.W. successive vent sectors. These authors concluded that & Waterbury, J.B., 1981. Procaryotic cells in the hydrothermal either some aspect of alvinellid biology was not apparent vent tubeworm Riftia pachyptila Jones: possible chemo- and long-distance dispersal occurs, or that the dynamics autotrophic symbionts. Science, NewYork, 213, 340^342. of vents on a spatial and temporal scale over geological Chevaldonne¨ , P. & Jollivet, D., 1993. Videoscopic study of deep- time allowed short-range dispersal to maintain gene £ow sea hydrothermal vent alvinellid polychaete populations: despite weak dispersal ability in alvinellids. biomass estimation and behaviour. Marine Ecology Progress To fully understand reproduction at vents and seeps Series, 95, 251^262. requires an integrated holistic approach. It is necessary to Chevaldonne¨ , P., Jollivet, D., Vangriesham, A. & Desbruye© res, understand all aspects of the reproductive cycle D., 1997. Hydrothermal-vent alvinellid polychaete dispersal in (Figure 2) as well as determining the e¡ects of advective the eastern Paci¢c. I. In£uence of vent site distribution, bottom currents, and biological patterns. Limnology and processes to and from vents and seeps. This is beyond the Oceanography, 42, 67^80. scope of an individual scientist and requires a collabora- Childress, J.J. & Fisher C.S., 1992. 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