Hydrobiologia 503: 9–19, 2003. ´ M.B. Jones, A. Ing´olfsson, E. Olafsson, G.V. Helgason, K. Gunnarsson & 9 J. Svavarsson (eds), Migrations and Dispersal of Marine Organisms. © 2003 Kluwer Academic Publishers. Printed in the Netherlands. Dispersal at hydrothermal vents: a summary of recent progress Paul A. Tyler1 & Craig M. Young2 1School of Ocean and Earth Science, University of Southampton SOC, Southampton SO14 3ZH, U.K. 2Oregon Institute of Marine Biology, University of Oregon, P.O. Box 5389, Charleston, OR 97420, U.S.A. E-mail: [email protected] Key words: dispersal, larvae, seeps, vents, Vestimentifera Abstract The discovery of hydrothermal vents along the Galapagos Rift in 1977 opened up one of the most dynamic and productive research themes in marine biology. In the intervening 25 years, hydrothermal vent faunas have been described from the eastern, northeastern and western Pacific, the mid-Atlantic Ridge and the Indian Ocean in the region of the Rodriguez Triple Junction. In addition, there is evidence of hydrothermal signals from the Gakkel Ridge in the Arctic, the central and southwest Indian Ridges and the Scotia Arc in Antarctica. Although often per- ceived as a continuous linear structure, there are many discontinuities that have given rise to separate biogeographic provinces. In addition, the intervening 25 years have seen a massive increase in our understanding of the biological processes at hydrothermal vents. However, how vents are maintained, and how new vents are colonised has been relatively poorly understood until recently. This review addresses the known larval development of vent-endemic invertebrates. The distribution of larvae in relation to the hydrothermal plume, and the ocean ridge in general, are discussed and the experimental evidence of larval longevity and transport are discussed using such variables as gene flow and larval development rates. The concept of larval dispersal along the mid-ocean ridge is discussed in relation to dispersal barriers and relates the known biogeography of hydrothermal vent systems to both local and evolutionary processes. Introduction the form of methane and hydrogen sulphide. At vents, hydrogen sulphide was available as a product of sea- The discovery of hydrothermal vents along the water passing through the fractured basalt of the mid Galapagos Ridge in 1977 forced marine biologists to ocean ridge, being heated, reacting chemically with reassess the energy available for primary production the surrounding rock and all the sulphate being re- in marine ecosystems. Up to that time, with a few duced inorganically to hydrogen sulphide (Van Dover, minor exceptions, all energy for primary production 2000). At seeps, hydrogen sulphide is made available was believed to derive ultimately from the sun in the by the bacterial reduction of sulphate using methane form of photosynthetic primary production. With the and the release of carbon dioxide and hydrogen sulph- discovery of hydrothermal vents, and subsequently ide (Sibuet & Olu, 1998). Hydrogen sulphide is also cold seeps, a new energy source was discovered that made available by the biological degradation of or- originated beneath the seabed. In the case of hy- ganic matter. Thus at seeps (and some vents) it is not drothermal vents, this energy source was hydrogen uncommon for the hosts of thiotrophs and methano- sulphide used by chemolithoautotrophic bacteria for trophs to live side by side, and, in some cases, bacteria primary production, the products of which could be capable of methanotrophy and thiotrophy can be found transferred to supply the nutritional requirements of in the same host. In addition, seeps may be fuelled by the host organism. The discovery of cold seeps further particulate organic matter from pelagic production or demonstrated that chemical energy could be used for by allochthonous organic matter carried into the sea by significant primary production, in this case, being in large rivers. 10 Chemolithoautotrophy was not unknown to marine Explorer Ridge and the Gorda Ridge in the Northeast ecologists, as chemosynthesis is known to be carried Pacific (Normark et al., 1982; Tunnicliffe et al., 1986; out by bacteria at the interface of anoxic and oxic Rona et al., 1990). During the mid-1980s, there was conditions such as in the Black Sea (Sorokin, 1964) extensive and successful exploration of the back-arc and in sediment, visible as a black layer (Gray, 1981). basins of the western Pacific, the first being the Manus However, vents and seeps were the first expression of basin (Both et al., 1986) (Table 1). major ecosystems being fuelled by chemosynthesis. Major vent sites were not discovered in the At- In the very first publications describing hydro- lantic until the dredging of the TAG hydrothermal thermal vents, the importance of vent maintenance sites in 1985 (Rona et al., 1986). Subsequently, seven through reproduction, dispersal and recruitment was sites along the northern part of the Mid-Atlantic Ridge recognised. Corliss et al. (1979) noted “there are many (MAR), south of the Azores have been discovered questions to be answered about these animal com- and described (Desbruyères et al., 2000), as well as munities. One concerns how they locate and colonize sites to the north of Iceland, although no fauna has new vents. It is clear that an individual vent area has been described from these last sites. Very recently, a finite lifetime”. In the intervening 25 years, there hydrothermal plumes have been observed south of As- has been a wealth of literature on the physiology, cension Island on the southern MAR (C.R. German, ecology, evolution and biogeography of hydrothermal pers. comm.). In the Atlantic, hydrothermal vents are vents (for reviews see Tunnicliffe, 1991; Childress generally widely spaced compared to the EPR. In the & Fisher, 1992; Van Dover, 2000; Van Dover et al., southern hemisphere, hydrothermal vents with fauna 2002) and also on cold seeps (Sibuet & Olu, 1998), occur at the Rodriguez Triple Junction in the Indian but study of the reproductive biology, dispersal and re- Ocean (Hashimoto et al., 2001; Van Dover et al., cruitment has been patchy (Tyler & Young, 1999). One 2001) and vent plumes have been discovered along of the most difficult aspects of studying the life-history the Southwest and Southeast Indian Ridge (Table 1) biology of vent organisms is the necessity to exam- (German et al., 1998; Scheirer et al., 1998). In the At- ine temporal processes, requiring visits to the remote lantic sector of the southern ocean, vent plumes occur sampling sites of vents at different times of the year. along the back-arc basin of the Scotia Arc (German This has had major logistical and fiscal constraints. et al., 2000). Lastly, in the Arctic, there is evidence of However, with programmes such as the EU-funded hydrothermal signals along the Knipovitch and Gakkel AMORES programme and the US-funded LARVE Ridges (Table 1), although a true vent fauna has not program considerable progress has been made in the been sampled (see Edmonds et al., 2003). last few years. In this mini-review, we address a number of as- pects that have led to our understanding of the dis- Biogeographic implications of vent discovery and persal at hydrothermal vents. We have concentrated on first indications of dispersal hydrothermal vents as they form part of the linear mid- ocean ridge systems and have a number of features that The discovery and faunal descriptions of vent are comparable. sites gave rise to the description of biogeographic ‘provinces’ and also gave the first indications of dis- persal (Van Dover et al., 2002). The biogeographic Distribution of known vent sites province identified first was that of the East Pacific Rise (Fig. 1), dominated by the tube worm Riftia The known distribution of vents is by no means pachyptila Jones, the bivalves Calyptogena magni- complete. Initial discoveries of vents were along the fica Boss & Turner, and Bathymodiolus thermophilus Galapagos Rift (Fig. 1). These were quickly followed Kenk & Wilson, together with a variety of smaller spe- by vent discoveries along the East Pacific Rise at 13◦ cies especially gastropod and polychaetes (Hessler & and 21◦ N, and 17–19◦ S, in the Guaymas Basin of the Smithey, 1983; Fustec et al., 1987). Gulf of California, and more recently at 9◦ N(Table With the discovery of vents in the Northeast Pa- 1) (Lonsdale, 1977; Corliss et al., 1979; Spiess et al., cific, the dominant tubeworm was Ridgeia piscesae, 1980; Hekinian et al., 1983; Lonsdale & Becker, 1985; together with the polychaete Paralvinella sulfincola Haymon et al., 1991). At the same time, vents were Desbruyeres & Laubier (Tunnicliffe et al., 1985, being discovered along the Juan de Fuca Ridge, the 1986). Species of Calyptogena and Bathymodiolus 11 Figure 1. Distribution of the main hydrothermal vent sites in the world ocean. Recent discoveries of vents or plume signals are identified, RTJ: Rodriguez Triple Junction; Kairei and Edmond hydrothermal vents; Sites with plume signals include Southwest Indian Ridge (SWIR), Gakkel Ridge (GK), Southern Mid-Atlantic Ridge (SMAR) and East Scotia Arc (ESA). The known biogeographic provinces are 1. East Pacific; 2. NE Pacific, 3. Atlantic (Azores); 4. Western Pacific; 5. Indian Ocean (Figure adapted from Desbruyeres` & Segonzac, 1997). were thought to be absent but there is evidence they of Bathymodiolus suggested that this genus is one of occur occasionally, but not to the extent of the EPR, the most widespread of vent and seep genera; it is the most notable site being Clam Acres on the Juan found in the EPR and the Atlantic, as well as the In- de Fuca Ridge. These differences give rise to the dian Ocean and is also common at cold seeps in the Northeast Pacific geographical province. Although the Gulf of Mexico (MacDonald et al., 1990). Vestimenti- MOR of the Northeast Pacific had been attached to feran tube worms are not found at any of the Atlantic that of the East Pacific in the geological past, separ- vents sites although vestimentiferan species are found ation by seafloor spreading had isolated the respect- at cold seeps in the Gulf of Mexico and the eastern ive communities such that dispersal could not main- Atlantic (Kennicutt et al., 1985; Dando et al., 1992).