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Biology of the vent crab Bythograea thermydron: a brief review.

ABSTRACT This paper provides a review of relevant literature concerning the vent crab Bythograea thermydron. This body of work describes a crab species that shares fundamental biological characteristics with typical shallow-water brachyuran crabs, yet possesses a suite of highly evolved traits specific for life at hydrothermal vents. Bythograea thermydron is one of only six known species of By thograea and is very abundant at vent sites along the East Pacific Rise. Because of the large amount of scientific work at this location, almost everything known about bythograeid vent crabs is based on studies of this single species. This review specifically deals with biogeography, systematics, and evolution; morphology, physiology and special adaptations; ovarian development; mating, brooding, and hatching; and larval biology and dispersal. The various sections emphasize comparisons with shallow-water crabs and highlight characteristics such as: (1) the unique eye structure in the adult stage, which is adapted for sensing the exceptionally dim light that is generated by the vents themselves; (2) the extreme tolerance of adults and juveniles to conditions of low oxygen and high sulfides; (3) the exceptional eurythermal character of juvenile and adult physiology; and (4) the seasonality of ovarian development and subsequent reproductive activity. Discussion of larval biology presents various scenarios of larval dispersal and recruitment back to the vent sites.

KEY WORDS: vent crab, Bythograea, zoea, megalopa, juvenile, hydrothermal vent

INTRODUCTION

The crab, Bythograea thermydron (Williams, 1980), is an important predator in hydrothermal vent communities in much of the eastern Pacific (Gorodezky & Childress 1994, Voight 2000, Micheli et al. 2002). The species was first described over 25 y ago (Williams 1980) and was immediately assigned to a new family (Bythograeidae) that now includes five genera and 13 species, all of which are restricted entirely to vent environments at depths ~2,500 m (Martin & Haney 2005). The genus Bythograea includes six species, some of which co-occur at the same vent sites. Bythograea thermydron is the most well-studied of these and is the dominant crab at vent sites spanning 40 degrees of latitude (~4,500 km) from ~20[degrees]S to 20[degrees]N along the East Pacific Rise about 1,000 km off the coasts of Central and South America. The species has also been reported from the Galapagos Rift (Martin & Haney 2005).

Adult morphology is characterized by a lack of external pigmentation and reduction of external eye structure (Williams 1980). Reproduction is typical of brachyuran crabs and includes apparent copulation, external brooding of eggs, planktonic zoea larvae, and a single megalopa stage (Van Dover et al. 1985, Jinks et al. 2002, Perovich et al. 2003) Growth and development of juveniles have been studied in the laboratory (Epifanio et al. 1999), and the approximate lifespan of adults (>4 y) has been determined in the field (Bennett & Turekian 1984). Adult physiology is unique in the extreme plasticity of thermal response (Mickel & Childress 1980, Childress & Fisher 1992), the unusual ability to detoxify sulfides (Powell & Somero 1986, Vetter et al. 1987), and an obligate dependence on high ambient pressure (Mickel & Childress 1982a, Airriess & Childress 1994).

Studies in our laboratory have centered on the reproductive biology and early life history of B. thermydron. In one of these investigations, we have described cyclical patterns in the maturation of gonads and in the extrusion and brooding of eggs (Perovich et al. 2003). In other work with early life-history stages, we have reported on swimming behavior of megalopae and on aspects of growth of early juveniles (Epifanio et al. 1999) and we have compared the quite unremarkable structure and function of zoeal eyes to the entirely unique structure and function of the juvenile and adult eye (Jinks et al. 2002). More recently we have used stable isotope techniques to infer trophic relationships among various life-history stages of B. thermydron and co-occurring species at vent sites along the East Pacific Rise (Dittel et al. 2005).

In this paper we provide a brief review of the biology of B. thermydron and use that opportunity to draw additional inference from some of our own work with the species. The remainder of the paper is organized in seven sections. In the first three sections, we consider systematics and evolution of the species, morphology of different life history stages, and general physiology. Following that, we offer a single section on ovarian development, followed by one segment dealing with brooding and hatching and another covering larval dispersal scenarios. In a final section we provide a summary and synthesis.

BIOGEOGRAPHY, SYSTEMATICS, AND EVOLUTION

Hydrothermal vents occur at irregular intervals along the global midocean ridge system and support unique communities of organisms that are dependent on chemosynthetic bacterial production. To live in these environments, vent fauna have evolved behavioral, physiological and morphological adaptations. Among these are distinctive adaptations to cope with extreme conditions of temperature, sulfides and metals (Arp & Childress 1980, Arp & Childress 1981). Thus, few vent species are found outside the immediate vent environment (Tunnicliffe & Fowler 1996).

Over 460 invertebrate species have been reported since vent communities were discovered in the late 1970s, and 82% of these are restricted entirely to vent ecosystems (McArthur & Tunnicliffe 1998). Whereas recognizing that some endemic hydrothermal vent taxa are relatively young, Newman (1985) proposed that many of the modern-day vent taxa have ancient origins dating back to the Mezosoic and Paleozoic. McArthur & Tunnicliffe (1998) reported similar findings and stated that "endemic genera, families, and higher taxa possibly reflect long term in situ radiation and evolutionary association with these sulfide-rich habitats." However, more recent studies, based on the fossil record and molecular phylogenies, have arrived at contrasting results and reject the hypothesis that vent fauna have Paleozoic origins (see review by Little & Vrijenhoek 2003). Instead, recent findings suggest a more recent origin of the vent fauna (Shank et al. 1999, Van Dover et al. 2001). In particular, Shank et al. (1999) reported that vent organisms like bresiliid shrimp are not remnants of a Mesozoic vent assemblage but instead seem to have radiated in the Miocene.

The ongoing discovery of new vent sites on a global scale since the early 1980s has allowed a better understanding of the biogeographic, evolutionary, and dispersal processes of vent fauna. Survey work has revealed that the degree of similarity in the faunal composition of vent communities from the various locations depends on the distance between vents and the history of the tectonic development (Fowler & Tunnicliffe 1997). That is, vent communities are always more similar to each other than to the adjacent nonvent communities, suggesting that dispersal of vent organisms generally occurs along the midocean ridge, rather than along other routes through the deep sea. Based on present day vent fauna and their relationships, it has been proposed that dispersal between the Atlantic and Pacific may be occurring today, most likely along the ridges in the Indian Ocean (Hessler & Lonsdale 1991, Fowler & Tunnicliffe 1997). For example, Hessler & Lonsdale (1991) reported that 59% of the 27 vent species from the Mariana Trough arc basin, show affinities with vent-endemic genera from the midocean ridge system; among these is Austinograea, a brachyuran crab belonging to vent-endemic family Bythograeidae. Similarly, the affinity between some Mariana Trough and Mid-Atlantic Ridge taxa suggest dispersal via the Indian Ocean (Martin & Hessler 1990). More recent work in the Indian Ocean supports these previous findings. For example, (Van Dover et al. 2001) reported geographic affinities among decapods like Rimicaris from Karei in the Indian Ocean vents and those of R. exoculata from the Mid-Atlantic. In turn, these authors also reported affinities between Indian Ocean and western Pacific taxa.

Vent communities worldwide are often characterized by the abundant occurrence of brachyuran crabs in the family Bythograeidae (Williams 1980). Currently the family consists of 13 species assigned to 5 genera (Guinot et al. 2002, Hessler & Martin 1989, Martin & Haney 2005). These genera include: Allograea (Guinot et al. 2002); Austinograea (Hessler and Martin 1989); Cyanograea (de Saint Laurent 1984); Bythograea (Williams 1980); and Segonzacia (Guinot 1997). Segonzacia has been found only in the Atlantic Ocean (Guinot 1997), whereas Austinograea, is distributed along the Western Pacific and Indian Ocean vents. The other three genera are known from the Eastern Pacific Ocean (Martin & Haney 2005). According to Guinot & Hurtado (2003), all bythograeid species display similar morphologies concerning carapace, mouthparts, and sternal plates, whereas major differences are found in eye structure and in the location of the antenna and antennules. In the present review, we focus on the most diverse of the genera, Bythograea, and more specifically on B. thermydron, the most widely studied species of this family of brachyuran vent crabs (Martin & Haney 2005).

There are six described species of Bythograea with a wide distribution along the East Pacific Rise (EPR) and Galapagos Rift (Martin & Haney 2005). Bythograea thermydron, is the most abundant species on the EPR, although it has not been found south of the Easter Microplate (~25[degrees]S) on the southern EPR (Guinot & Segonzac 1997, Guinot & Hurtado 2003). Bythograea microps (de Saint Laurent 1984), has been found between 10[degrees] and 13[degrees]N on the EPR, whereas B. laubieri (Guinot and Segonzac 1997) is found only in vents on the southern EPR between 11[degrees]S and 21[degrees]S (Guinot & Hurtado 2003). The most recent descriptions are the species B. galapagensis and B. vrijenhoeki (Guinot & Hurtado 2003). The former is known only from the type locality (eastern Pacific Ocean, Galapagos Rift), whereas the latter is found both in the type locality and in the immediate vicinity, south of the Easter Microplate (Guinot & Hurtado 2003). One additional species, B. intermedia, was first described by de Saint Laurent (1988) (in Martin & Haney 2005). However, this apparent species is based on a small number o f juvenile specimens and is considered of questionable status (Guinot & Hurtado 2003, Martin & Haney 2005).

Williams (1980) placed B. thermydron in an independent superfamily (Bythograeoidea), whereas acknowledging characters suggestive of portunoid and xanthoid affinities. Bowman & Abele (1982) agreed by placing Bythograeids between the superfamilies Portunoidea and Xanthoidea. In recent years, different approaches have been used to examine the phylogenetic origin of Bythograeid crabs. Whereas some studies have presented similar conclusions and provided further information about the possible origin and evolution of vent crabs, others have reported contrasting results. Thus, the issue remains controversial. For example, studies of sperm ultrastructure revealed similarities among three genera of Bythograeids (Bythograea, Austinograea, Segonzacia) and the deep-water trapezoid crab, Calocarcinus africanus (Calmon, 1909), but this finding was tempered by the additional finding that spermatozoa of C. africanus have a number of unique characteristics and appear structurally different from the spermatozoa of other trapezoids (Tudge et al. 1998). This complicating factor led the authors to propose that C. africanus be included with the bythograeids sensu late and hypothesized that bythograeids may have originated from Calocarcinus-like deep water xanthoids that entered the hydrothermal vent environment during the Eocene.

Leignel et al. (2007) arrived at similar conclusions after identifying and comparing the 70-kDa heat shock protein (HSP70) genes from three genera of bythograeids with xanthid crabs. Accordingly, these authors suggest that the presence of similar members of the HSP70 family found in vent and xanthid crabs could be considered as an ancestral character and concluded that xanthids and bythograeids are more closely related to each other than to trapezoid crabs. In a study of the osmoregulatory capabilities of B. thermydron, Martinez et al. (2001) concurred with previous authors regarding the phylogenetic origins of the vent crab. Because B. thermydron is a marine osmoconformer (unlike its prosposed ancestors), Martinez et al. concluded that vent crabs possibly lost the osmoregulatory abilities after conquering salinity-stable environments like the vents. In contrast, analysis of crustacean hyperglycemic hormone (CHH) and the structure of its cDNA precursor have suggested a possible phylogenetic relationship between Bythogaeidae and Cancridae, another osmoconformer (Toullec et al. 2002).

According to McArthur & Tunnicliffe (1998), much of the hydrothermal vent fauna has mosaic origins and possibly invaded these ecosystems throughout the Paleozoic, Mesozoic, and Cenozoic. In the case of vent crabs, Guinot & Segonzac (1997) cite A. B. Williams as suggesting that crabs in the superfamily Bythogreaoidea diversified in the Cenozoic, although most other brachyuran superfamilies originated in the late Mesozoic (McArthur & Tunnicliffe 1998). To date, no arthropod fossils have been found at historical vent sites, but there is evidence that crustaceans lived in chemosynthesis-based communities in the past and thus may have been present in ancient vent communities (von Bitter et al. 1992, Little et al. 1998).

MORPHOLOGY

Morphology of Zoeae and Megalopae

Female B. thermydron produce large numbers of relatively small eggs (~0.5 mm diameter), which are brooded on the ventral surface of the abdomen in typical crab fashion (Williams 1980, Van Dover et al. 1984, personal observations) (Fig. 1). Whereas the high fecundity and small eggs observed in B. thermydron suggest that development includes planktotrophic instars (Van Dover et al. 1985), we know little about zoeal development (e.g., number and duration of larval stages, swimming behavior etc.) of vent crabs. Stage I zoeae have been observed only a few times in the water column near vent sites, and, no intermediate stages have ever been collected. Nonetheless, the large difference in the respective sizes of stage I zoea (1.5 mm total length) and the postlarval megalopa stage (7.5 mm) implies that normal larval development includes as many as seven or eight zoeal stages (Van Dover et al. 1984, Van Dover et al. 1985, Martin & Haney 2005). To date, the only description of a zoeal stage is based on a single specimen collected in a plankton tow at the 21[degrees]N vent site (Van Dover et al. 1984).

[FIGURE 1 OMITTED]

According to preliminary observations made by Van Dover in 1984, eggs hatch as a prezoea or zoea with premature zoeal characters. In our own investigation, we were able to hold an ovigerous female crab under hyperbaric conditions until its eggs hatched. Newly released larvae appeared to have undeveloped maxillipeds--the exopods were lacking setae--but showed the characteristic ornamentation of the zoea I (see below). Rostral and dorsal spines were in an erect position (Fig. 2) rather than the folded position observed in the prezoea stages of other brachyuran crabs (e.g., Davis 1965, Clark et al. 1998). Whereas we were unsuccessful in culturing the larvae, zoeae survived for one week at atmospheric pressure, though there was no indication of any further development.

We also removed eggs from ovigerous females and kept them at room temperature and atmospheric pressure for several hours. Observation under a stereo-microscope showed that larvae emerged from eggs in an apparent prezoeal stage. Whereas the normal occurrence of a free-living prezoeal stage under natural conditions remains controversial (Clark et al. 1998), there are many reports of its occurrence in the laboratory. For example, Gore (1985) described the existence of the prezoea stage in many families of shallow-water brachyuran crabs where the stage may last only a few minutes before molting into a "normal" stage I zoea (Davis 1965). However, the prezoeae that we observed at atmospheric pressure did not exhibit any signs of further development, and there remains the possibility that the larvae hatched in a premature stage because of the stress of laboratory conditions.

[FIGURE 2 OMITTED]

Based on observation of a single specimen of field-caught larvae, Van Dover et al. (1984) reported that stage I zoeae of Bythograea have unique features that distinguish them from other brachyuran larvae. For example, the arrangement and extraordinary number of spines and processes on the carapace, abdomen and telson of vent crab zoea are distinctive. Another distinguishing characteristic is the lack of asymmetry in the setation of the exopodites of the 1st maxillipeds of these larvae with respect of other brachyuran crabs. With the exception of dark brown eyes, Van Dover (1984) reported lack of pigmentation of the zoea. In contrast, our observations showed that newly released prezoeae had distinct pigmentation around the eyes and thorax (Fig. 2).

Considerably more information is available about the morphology, physiology and behavior of the megalopa and adult stages. In a recent paper, Martin & Dittel (2007) provided a detailed description of the megalopal stage of B. thermydron and concluded that there are no obvious morphological adaptations specific to existence in vent environments. As with the megalopae of most brachyuran crabs, the morphology of their mouthparts and chelae equips B. thermydron megalopae to capture zooplankton in the water (although there is no information concerning actual diets in nature). However, in contrast to many other brachyuran species, B. thermydron megalopae lack distinctive family-specific characters such as the large sternal spines in some portunid megalopae or the recurved hooks found on the chelipeds of some xanthids and cancrids (Martin et al. 1998). According to Martin & Dittel (2007), the lack of specialized or unique features may be indicative of a primitive position relative to other brachyuran crabs.

Nonetheless, B. thermydron megalopae are unusual in the crab-like shape of their carapace, extremely large size (>8 mm carapace width), and in their bright red coloration (Williams 1980; Fig. 1). Moreover, (Jinks et al. 2002) reported that B. thermydron zoeae and megalopae larvae possess image-forming compound eyes with a visual pigment well suited to wave lengths characteristic of dim sunlight and bioluminescence in the mesopelagic and bathypelagic regions of the water column (see section on Larval Biology and Dispersal below).

Morphology of Juveniles and Adults

In his initial description of Bythograea, Williams (1980) included observations of the megalopa and juveniles. Williams (1980) reported the size of a limited number of specimens consisting of seven megalopae and six juvenile crabs (average carapace width: 6.51 mm [+ or -] 1.3 and 6.5 mm [+ or -] 0.3, respectively) and noted that there are dramatic ontogenetic changes from the 1st juvenile crab stage to the adult. For example, the ocular area becomes broadened with increasing width of the carapace; the subocular plate and the epistome are gradually projected forward and the eyestalks degenerate. Also, the interantennular septum is completely absent in the megalopa, and the septum is barely visible at the upper and lower edges between the two antennular fossae in the largest juveniles. The author suggested that the lack of development of this structure is probably related in part to the loss of sight. In fact, recent studies have demonstrated that a remarkable adaptation to life in the vents is the transformation and reduction of the eyes of juvenile and adult vent crabs (Jinks et al. 2002). After megalopae settle and metamorphose, the compound eye is replaced with a naked-retina eye in the first juvenile crab stage, allowing the crabs to sense the dim light produced by various chemical and biochemical processes at the vent sites (Jinks et al. 2002).

Williams (1980) also stated "that the smallest juvenile crab stages are smaller than the larger megalopae." However, more recently, field and laboratory studies have provided better estimates of carapace widths, dry weights and stage duration of early juvenile stages. Epifanio et al. (1999) were successful in rearing megalopae and juveniles; six megalopae molted successfully to juvenile stage and two of these individuals survived through at least one more molt stage in the laboratory. In addition, 14 field-collected juveniles of various sizes underwent at least one molt in the laboratory; 9 of these initiated a second molt and one individual survived through three molts. Based on this information, the authors performed analysis of coordinates for carapace width and carapace length and reported an increase in carapace width from approximately 8 mm at Stage 1 to around 22 mm by Stage 5. In addition, the carapace width of megalopae in that investigation was considerably larger than that reported by Williams, and in contrast to observations by Williams, first stage juveniles were in all cases larger than the megalopa stage. The average width of the megalopae and juvenile Stage 1 were 7.9 mm [+ or -] 0.3 (n = 73) and 9.3 mm [+ or -] 0.3 (n = 42), respectively; dry weight increased from about 40 mg in the 1st juvenile stage to nearly 270 mg by the 5th stage.

The reason for the large difference in size of specimens in these two studies is not clear. Whereas specimens described by Williams were collected in the Galapagos Rift (Rose Garden), and those from Epifanio et al. (1999) were from the northeastern Pacific Ocean (EPR, 9[degrees]N), it is difficult to believe that such large differences are caused by differences in collection sites. Martin & Dittel (2007) also observed several specimens of small megalopae (3.2 mm CW; 3.1 mm CL) in a collection from the Natural History Museum, London. The large size difference between these megalopae and the larger megalopae (7.5 mm) described by Epifanio et al. (1999) was surprising, especially because Epifanio et al. confirmed the species of the megalopae in that investigation using molecular techniques. Accordingly, it is possible that the small megalopae in Williams (1980) were misidentified as B. thermydron and were in fact the megalopae of a smaller co-occurring species, B. microps. In previous unpublished studies, one of us (AD) has collected megalopae as small as 2.6 mm that presented the same general morphological characteristics of B. thermydron. Several of these small megalopae molted to the 1st juvenile crab stage in the laboratory with carapace widths considerably smaller than the 1 st juvenile stage of B. thermydron (Dittel, unpublished data). Except for the difference in size, megalopae of these two species were indistinguishable using standard external morphological characters.

Studies by Epifanio et al. (1999) also revealed that the duration of the first juvenile stage was around 15 d under laboratory conditions (20[degrees]C, 1ATM) and increased considerably in subsequent stages (30-40 d) but with substantial variation among individual crabs. However, these estimates were insufficient for use in determination of growth rates because of a limited number of individuals and high variation in stage duration.

Morphology of Adult Crabs

Williams (1980) described the genus Bythograea, type species B. thermydron, as having a general cancroid aspect, characterized by a broad, depressed, and transversely elliptical carapace with indistinct regions; an anterolateral region produced and spineless. The front is of moderate width, slightly produced and bilobed. The orbits are incomplete and the supraorbital margin is short in adults. Other characteristics include a nearly horizontal suborbital plate and almost fully visible in dorsal view in adults and subadults, but incompletely developed in early crab stages. Also, the third maxillipeds have long setose palps. Chelipeds are moderately unequal, the section of the cheliped known as the hand is inflated, and walking legs have pointed dactyls. Segments 4 and 5 of the male abdomen are partly fused, whereas the mature female abdomen is broad with free segments and biramous pleopods on segments 2-5.

With the discovery and description of new species of Bythograea, it has become apparent the genus falls into two distinct groups: B. thermydron and B. galapagensis, which cohabit at the Galapagos Rift and B. laubieri and B. vrijenhoeki, which cohabit in the area near the Easter Microplate (Guinot & Hurtado 2003). The authors support this relationship based on one of the most reliable characteristics for distinguishing brachyuran species: the first male pleopods. In the case of this genus, the shape of the first male pleopods is twisted and S-shaped in the former group, whereas it is nontwisted in the latter. Additional characteristics such as the patterns of setation of walking legs allow distinction of the four species. The authors also compared the previous four species with B. microps, the smallest among the genus (24 mm in carapace width) the species with the most drastic reduction of eyestalks.

PHYSIOLOGY AND SPECIAL ADAPTATIONS

Various aspects of the physiology of adult B. thermydron have been studied extensively and have revealed adaptations that allow B. thermydron to exploit the entire vent environment from the oxygen-rich, 2[degrees]C water at the vent periphery, to the anoxic, 30[degrees]C water at the vent orifice. The largest body of literature in this area probably concerns B. thermydron's oxygen consumption and regulation. Early studies showed that variations in temperature and pressure, as experienced in the crab's normal range, had little effect on oxygen consumption rates (Mickel & Childress 1982a). Subsequent studies examined B. thermydron's mitochondrial respiration directly, also finding that it was more resistant

to high temperatures than those of related shallow water species (or even vent species that only experienced cooler waters of a steadier nature), suggesting that differences in thermal adaptations among endemic vent species are correlated with conditions prevalent in the microhabitat in which the organism resides.

Additional studies complimentary in nature investigated the function of the crab's respiratory protein, hemocyanin. Arp & Childress (1981) carried out experiments using the whole blood of B. thermydron. They reported that the hemocyanin of B. thermydron had a modest oxygen affinity, which was independent of temperature over the range of 2[degrees]C to 30[degrees]C, and a large carrying capacity in comparison with other crustaceans. This study also described a moderate, normal Bohr Effect, where oxygen affinity was moderately affected by pH and more strongly affected by C[O.sub.2] and concomitant changes in pH. In subsequent work with purified B. thermydron hemocyanin, Terwilliger & Terwilliger (1985) reported that the protein was structurally similar to those of nonvent brachyurans, but exhibited an unusually high oxygen affinity, higher even than that previously reported for whole B. thermydron hemolymph. Finally, Sanders et al. (1988) again investigated the effects of pH and temperature on hemocyanin binding, using dialyzed blood, and reanalyzing some of the original data reported by Arp & Childress (1981). Although this study did not corroborate the high values reported by Terwilliger & Terwilliger, it did provide improved resolution, reporting that oxygen affinity increases with increasing temperatures up to 10[degrees]C and then declines again at higher temperatures. Thus, for B. thermydron at lower temperatures, the Bohr Effect will compensate for the decrease in oxygen affinity that is present at temperatures below 10[degrees]C. At the higher temperatures, as pH and oxygen partial pressure decrease, B. thermydron has been shown to compensate by increasing its ventilation rate (Mikel & Childress 1982a). It is at these temperatures, in the anoxic vent water near the orifice, that the lowered oxygen binding affinity may be adaptive, allowing for an efficient release of oxygen molecules to meet tissue demand. Taken as a whole, this body of work describes an oxygen transport system that allows B. thermydron to maintain a suitable level of aerobic metabolism across the entire range of conditions encountered in the vent environment.

Other studies have delved further into elucidating the structure of B. thermydron hemocyanin. Markl & Decker (1992) reported that arthropod hemocyanins generally occur as hexamers and oligohexamers assembled from 75 kDa polypeptide chains, each one housing a single binding site for oxygen. Zal et al. (1996) used gel filtration to illustrate that the hemolymph of B. thermydron was comprised of a mixture of monomers, hexamers, dodecamers, and octodecamers; and these results were later confirmed using electrospray ionization mass spectrometry (ESI-MS) (Zal et al. 2002). A comparative study by Sanglier et al. (2003) concluded that associations of the oligomeric subunits that make up the hemocyanin vary according to the crab's environment. Because differences in these self-assemblies have implications for the oxygen binding properties of this respiratory pigment, this finding illustrates yet another way in which B. thermydron is able to adapt to changes in its microhabitat and exploit areas with variable oxygen concentrations.

Another body of literature explores how B. thermydron mitigates sulfide toxicity. Initial investigations into the pathways of energy metabolism of the crab by Hand & Somero (1983) revealed that the enzymatic activities found in its tissues were qualitatively and quantitatively similar to those of phylogenetically related shallow-living marine species. That is, the authors found no evidence of specialized, sulfide-insensitive cytochrome oxidase systems, and those present in the crab were still half-inhibited by hydrogen sulfide like their shallow-water counterparts. Vetter et al. (1987) determined that B. thermydron was able to oxidize sulfide into the less-toxic byproducts of thiosulfate and sulfate in its hepatopancreas. The thiosulfate accumulates in the hemolymph where it has actually been shown to increase hemocyanin-oxygen affinity, similar to increases seen with L-lactate (Sanders & Childress 1992). Subsequent studies that experimentally exposed crabs to sulfide showed the expected increase in thiosulfate in the hemolymph and an increased ability to regulate oxygen consumption in conditions where concentrations were low (Gorodezky & Childress 1994). These authors concluded that the enhanced ability to regulate oxygen consumption could imply that increased hemocyanin-oxygen affinity caused by elevated thiosulfate may be an adaptive response used by the crab in the vent environment, allowing the crab to forage in the areas of high faunal densities associated with the warm, sulfide-rich waters surrounding the vent orifice.

Although it is doubtful that the crabs experience drastic extremes in pressure variation within their natural habitat, the study of these organisms has inevitably exposed them to pressures that yield insight into their physiological tolerances. For some deep-sea organisms, at the cellular level, there is a shift in membrane lipid composition with increasing depth. This shift maintains membrane fluidity in the face of increasing pressure, which would tend to order the membrane lipids. If this type of adaptation were indeed used by Bythograea, a decrease in pressure (which decreases the viscosity of phospholipid membranes) would be ameliorated by a temperature reduction (which causes an increase in membrane viscosity). Conversely, one would expect that increased pressure would be counteracted by a temperature increase. It is exactly this type of pressure-temperature interaction that was shown to occur in B. thermydron in response to experimental changes in pressure, implicating that there is a homeoviscous mechanism at work in which phospholipid membrane fluidity is affected by external pressure disturbance (Airriess & Childress 1994). This finding corroborates our own observations in rearing the crabs. When maintaining the crabs onboard ship and in the laboratory, lower temperatures appeared to reduce the neuromuscular dysfunction that resulted from the abrupt changes in pressure that were unavoidable in the care and feeding of the animals held in pressurized aquaria. Furthermore, it was also our general observation that, regardless of temperature, larvae and juveniles were less affected by changes in pressure than adults (see Larval Biology and Dispersal section below).

In general, the physiological observations described in this section provide us with insights into the ecology and behavioral dynamics of B. thermydron. It has been hypothesized that stable, low oxygen environments (such as the midwater oxygen minimum layer) select for aerobic adaptations, whereas unstable low oxygen environments select for anaerobic adaptations (Mikel & Childress 1982a). This is certainly true for B. thermydron whose existence in the highly variable vent environment has led to a moderate aerobic capacity and a considerable anaerobic capacity. This anaerobic capability allows them forage for long periods in the warm anoxic water at the vents. Their ability to tolerate a wide range of temperatures allows them to move throughout the entire vent habitat, periodically moving into the colder water at the vent periphery where brooding and hatching of eggs occurs (Perovich et al. 2003). In addition, the juvenile and adult stages are relatively insensitive to changes in pressure, and available evidence indicates that the crab could survive at depths as much as 2,000 m shallower than typical vent sites. Thus, the distribution of B. thermydron around the vents is less likely determined by their physiological capabilities than it is a result of behavioral patterns evolved in response to selection by ecological factors.

OVARIAN DEVELOPMENT

Perovich et al. (2003) conducted a study of the reproductive biology of B. thermydron at several vent sites along the East Pacific Rise that provided insights into spatial and temporal variations in ovarian development. This study also provided the first detailed histological analysis of ovarian structure for this species.

On gross examination, the ovaries of B. thermydron are actually visible through the thin white carapace, especially in the more mature stages. After dissection, the ovary was found to exhibit bilateral symmetry with the main ovarian lobes positioned dorsal to the hepatopancreas, actually obscuring the hepatopancreas from view when in an advanced reproductive stage. As is typical for brachyuran crabs, the ovaries extend along the anterior margins of the cephalothorax, running posteriorly through the body cavity to the seminal receptacles. The oviducts pass ventrally from the seminal receptacles to open onto the ventral surface of the body. In a mature animal, these are relatively easy to see. In an immature individual, or in an organism that has just spawned, the ovaries appear as thin strands of clear or white tissue that are difficult to see and remove.

The study went on to show that as vitellogenesis commences, the ovaries become greatly enlarged. They change in color from clear, to white, to light pink, to a bright fuchsia, whereas simultaneously taking on a pebbled appearance that is the result of its many lobes now swollen with large ova. The entire ovary is enclosed by a thin capsule of fibrous connective tissue and associated cells, which separates the ovary from the rest of the coelomic cavity. The germinative centers, where all cell division takes place, are composed of oogonia that run in strands longitudinally throughout the ovary. The youngest oocytes arising from the oogonia measure about 15 [micro]m (feret diameter). Previtellogenic oocytes do not contain much cytoplasm, and the small amount present is dense and basophilic, causing the cells to stain a deep blue to purple. The nuclei are large in reference to cell volume, and more than one nucleolus was frequently observed (usually 2-3).

The study also documented the onset of vitellogenesis, which occurs when cells reach approximately (150 [micro]m). At the beginning of vitellogenesis, yolk inclusions are confined to one hemisphere of the oocyte. As vitellogenesis progresses, the yolk granules gradually fill the entire cell, with larger inclusions located toward the periphery of the oocytes. At completion of vitellogenesis, oogonia, and previtellogenic oocytes still remain along the germinative strands, ready to create the next cohort of mature oocytes (Fig. 3).

Overall, the results of Perovich et al. (2003) indicate that the histological characteristics of egg development in B. thermydron do not differ significantly from shallow-water forms (Johnson 1980). Moreover, the oocyte size-frequency distributions for B. thermydron individuals clearly demonstrate group-synchronous gametogenesis within the gonad (i.e., at least two modes of oocyte sizes are present during most of the reproductive cycle). This suggests an iteroparous reproductive strategy wherein the ovaries contain an immature cohort characterized by previtellogenic oocytes and oogonia and a second cohort that eventually undergoes vitellogenesis and matures. Only one cohort matures within the ovary at any given time. This pattern of development is typical of brachyuran crabs in general and has been reported in other species of deep-sea crabs (Haefner 1977) and in vent shrimp (Ramirez-Llodra et al. 2000).

[FIGURE 3 OMITTED]

Perovich et al. (2003) also documented a significant difference in mean size of oocytes among groups of crabs collected in the three respective sampling periods, suggesting periodicity in the reproductive cycle of the vent crab. Two samplings, done in subsequent years, but both in the month of May, were similar to one another. Females collected in these samplings exhibit a dominance of previtellogenic oocytes with a second, smaller group of vitellogenic oocytes present. In contrast, a November sampling contained females exhibiting a wide variety of oocyte sizes within their ovaries, with no one size class predominating. The November data are indicative of a population comprised of individuals exhibiting various stages of maturity, whereas the May samples are indicative of the end of a spawning period. This led the authors to suggest a spawning cycle where peak spawning occurs in April to May, characterized by the high percentage of females bearing evidence of recent brood release in both May samples and a preponderance of previtellogenic oocytes within the population. A seasonal reproductive cycle was documented for the deep-water crab, Chaceon (Geryon) quinquedens (Smith 1879), despite the fact that ovigerous females were captured in all seasons (Heafner 1978). Likewise, annual reproductive cycles showing peaks of egg bearing have also been documented for shallow-water brachyurans (Haddon & Wear 1993). Additionally, Erdman et al. (1991) suggest that whereas Chaceon fenneri (Manning & Holthuis 1984) and C. quinquedens reproduce annually at the population level, some individuals may reproduce biennially. More difficult to ascertain, however, are the reasons behind such a pattern in an environment of constant food supply and devoid of any marked seasonality.

In general, little is known about the endogenous or exogenous factors that control reproductive cycles in the deep sea (Company & Sarda 1997). Schoener (1968) first suggested that variation in the flux of particulate food material to the deep sea might cue seasonality in reproductive activity. In recent years, this idea has been recast as the phytodetrital-flux hypothesis, wherein variation in the flux of surface-produced particulate material to the sea floor would serve as the cue for seasonal spawning (Gage & Tyler 1991).

Tyler et al. (1982) observed that several deep-sea echinoderms from the Rockall Trough in the northeastern Atlantic basin produced planktotrophic larvae and synchronized their time of spawning to occur simultaneously with the sinking of organic matter from the phytoplankton bloom that occurs each spring in surface waters above the trough. In contrast, this synchronization was absent in co-occurring echinoderms whose mode of larval development is lecithotrophic. More recently, a relationship has been demonstrated between the onset of vitellogenesis and the sinking of phytodetrital matter in Leucon profundus, an abyssal cumacean, also from the Rockall Trough (Bishop & Shalla 1994). In addition, field and laboratory experiments involving the majid crab Chionoecetes opilio have shown that larval release was linked to phytodetrital deposition (Starr et al. 1994).

In fact, phytoplankton blooms occur seasonally (spring and summer) in the surface waters of the tropical Eastern Pacific (Longhurst 1993) and sediment analysis has shown that phytodetritus reaches the seafloor in this area in amounts that could yield significant contributions to the annual carbon budget of the benthic community (Smith et al. 1996). However, the authors also reported that chlorophyll-rich detritus was only found from 5[degrees]S to 5[degrees]N, with the highest concentration within 2-3[degrees] of the equator and sediment samples at 9[degrees]N revealed a brown flocculent material that contained very few diatom remains, little chlorophyll, and few zooplankton fecal pellets. Accordingly, it does not seem likely that phytodetrital flux, per se, plays a major role in the reproductive biology of B. thermydron by providing a benthic food source for the adults themselves, because this flux is negligible compared with the autochthonous production at the vents. However, recent research suggests that larval development in B. thermydron is planktotrophic (Van Dover & Trask 2000) and that the larval stages of appear to have wide tolerance for variation in temperature and pressure and have the physiological potential to exploit a large portion of the water column over the vents (Epifanio et al. 1999, Jinks et al. 2002). Therefore, variation in surface production may have a direct effect on the nutritional environment to which the larvae are exposed and thus, an indirect effect on seasonality of reproductive activity in the adults.

MATING, BROODING, AND HATCHING

Fertilization in brachyuran crabs typically includes copulation that often occurs immediately after the female has molted (Epifanio 2007). The male deposits sperm packets in the seminal receptacles of the female, providing her with the potential to fertilize more than one batch of eggs. Clusters of fertilized eggs are eventually deposited on abdominal appendages known as pleopods and are brooded externally until hatching. In shallow-water crabs, the time from extrusion of eggs until hatching varies widely among species and ranges from a few days to several months. Whereas B. thermydron presumably demonstrates a similar pattern of copulation and fertilization, mating has never been observed and ovigerous females are rarely seen at the vent orifice. It is not known how long B. thermydron females brood their eggs.

Because ovigerous crabs are rarely observed near vent orifices, it had been assumed that female crabs occupy habitat on the periphery of the vent fields during the mating and brooding period (Epifanio et al. 1999). This assumption was verified by Perovich et al. (2003) who demonstrated that ovaries of females collected immediately adjacent to a vent were dominated by intermediate stage oocytes, whereas those collected from the periphery of the vent field contained only earlystage and mature-stage oocytes. These authors concluded that the early-stage oocytes would support the succeeding year's reproductive activities, whereas the mature oocytes would be fertilized in present mating activities at the peripheral site. This conclusion was supported by collections from the peripheral site, which were dominated by females that were either brooding eggs or showed clear evidence of recent hatching of eggs, and by high proportion of females compared with males at the peripheral sites. Thus, it appears that mature females migrate to the vent periphery where they may copulate with itinerant males and eventually extrude, brood, and hatch their eggs.

It is not clear why females leave the vent-orifice region to brood and hatch their eggs. However, the lack of brooding females in the region adjacent to the actual vents has also been reported for one species of hydrothermal vent shrimp (Rimicaris exoculata Williams & Rona 1986) from the Mid-Atlantic Ridge (Ramirez-Llodra et al. 2000). Earlier work with various species of the deep-sea crab Geryon (now Chaceon) has also documented a migration of brooding females away from the general population of adults (Haefner 1978, Melville-Smith 1985). Thus, there may be some general advantage to this type of behavior. The simplest explanation for B. thermydron is that high temperatures at the vent orifice, combined with vent fluids rich in sulfide and heavy metals, may be toxic to larvae. Additionally, the vent periphery does not have the dense aggregations of biota that characterize the near-orifice region, and predation on newly hatched larvae would likely be minimized in the peripheral zone.

There has been only one in situ observation of an ovigerous female vent crab (presumed to be B. thermydron) in the act of hatching eggs in a vent peripheral zone of the East Pacific Rise (C. Van Dover, Duke Marine Laboratory, Beaufort, NC; pers. comm.). Additional in situ observations were made from the deep submersible Shinkai 6500 on the Southern East Pacific Rise (Ytow, University of Tsukuba, Ibaraki, Japan; pers. comm.) that included a description of eight gravid bythograeid females congregating on barren rock approximately 50 m away from the nearest vent site, "fanning," or ventilating their abdomens as zoea larvae hatched from the brooded eggs. In our laboratory, we have observed egg hatching in several ovigerous females held in hyperbaric aquaria at a pressure of 150 atmospheres. These larvae appeared to have been hatched prematurely, and their morphology differed from that expected for a first-stage zoea form in that maxillipeds were devoid of natatory setae (see Morphology section above). Because of this deficiency, the zoeae were unable to swim and appeared unable to grasp prey items. We were unsuccessful in culturing these premature zoeae in the laboratory.

The cause of premature hatching was not clear, but the ovigerous females had been subjected to considerable handling before they arrived in our laboratory. These individuals had been collected in traps at vent sites along the East Pacific Rise and held in hyperbaric aquaria onboard ship until they were shipped from the west coast of Mexico via air freight to our laboratory on the east coast of the United States. Accordingly, both the females and their brooding eggs experienced at least 48 h at surface pressure before they arrived in our laboratory. This period of low hydrostatic pressure may have impacted the normal pattern of development in the eggs.

LARVAL BIOLOGY AND DISPERSAL

Stage I zoea larvae of B. thermydron have been collected only rarely in the vent-site water column and differ from shallow water forms in their unusually extensive spination (see Morphology section above). More advanced zoeae have not been observed in nature, and the typical number of zoeal stages is unknown. However, the large difference in size between the first zoeal stage and the megalopa stage suggests a relatively large number of zoeal stages (see Morphology section). For example, various species of shallow-water blue crabs in the genus Callinectes have a similar disparity in size between the first zoeal stage and the megalopal stage (Kennedy 2007)--and these species typically have seven or eight zoeal stages (Epifanio 2007). This is in contrast to shallow-water mud crabs in the family Xanthidae wherein stage I zoea are relatively large compared with the megalopal stage and where development typically consists of four zoeal stages (Welch & Epifanio 1995).

Some insight into the field distribution of B. thermydron larvae can be gained from studies of their eye structure and visual pigments. Recent investigations of the species indicate that stage I zoea larvae possess image-forming compound eyes with a visual pigment sensitive to blue wavelengths typical of mesopelagic waters at depths ~1,000 m (Jinks et al. 2002). This is in contrast to shallow-water species where visual sensitivity is shifted to yellow-green wavelengths typical of coastal regions (Cronin & Jinks 2001) and to the vent sites themselves where sunlight at visible wavelengths is no longer apparent (Land 1989). Thus, it appears that vision in B. thermydron zoeae may be adapted to a distribution in the mesopelagic plankton, some 1,500 m above the vent sites. This bit of evidence fits well with the observation that B. thermydron zoeae are released in the peripheral zone and may not be entrained in the vent plume, which is usually advected along the rift valleys a few hundred meters above the bottom, but instead may migrate to higher positions in the water column extraneous to the plume (Kim & Mullineaux 1998).

On molting to the megalopal stage, the maximum sensitivity of B. thermydron's visual pigments shifts to blue-green wave lengths (Jinks et al. 2002), which may be an adaptation to detect bioluminescence in deeper bathypelagic waters, adjacent to the vent sites (Frank & Case 1988). Near the bottom, hydrothermal vents generate dim light in the near IR and visible portions of the spectrum (White et al. 2002). The naked-retina eyes of the early juvenile crab stages of B. thermydron are capable of sensing very dim light in this part of the spectrum and may serve as photon-gradient detectors, supplementing chemical and thermal senses for proper orientation toward the vents during settlement and assisting in the selection of an appropriate habitat for juvenile life (Jinks et al. 2002, see Morphology section above).

Bythograea thermydron megalopae and juveniles also show behavioral and physiological characteristics that support the idea of larval development in the water column extraneous to the vents. Epifanio et al. (1999) have shown that megalopae larvae survive and undergo metamorphosis at pressures ranging from ambient-surface to at least 260 atmospheres ([approximately equal to] 26 MPa). Moreover, the early juvenile stages in this study exhibited this same tolerance for wide variation in pressure and have survived at atmospheric pressure for periods as long as six months, whereas undergoing as many as three molts. This is in contrast to the adult form of B. thermydron, which suffers cardiac dysfunction, loss of motor coordination, and eventual death on decompression to surface conditions (Mickel & Childress 1982a, see Physiology section above). Thus, the tolerance of relatively low hydrostatic pressures appears to be restricted to the early life history stages (presumably including the zoeal stages) and provides the potential for a great deal of flexibility in the vertical position of the zoeae and megalopae in the water column. The wide pressure tolerance of the early juvenile stages is probably a carry-over from larval development and, in any event, is lost in the later juvenile stages.

Megalopae larvae of B. thermydron are also tolerant of a wide range of temperature, even with minimal acclimation (Epifanio et al. 1999). This tolerance is clearly adaptive for organisms living at vent sites and has been well documented in adult B. thermydron and other vent species (Mickel & Childress 1982b, Dahlhoff et al. 1991, see Physiology section above). In behavioral experiments in our laboratory, B. thermydron megalopae showed active swimming behavior over the wide range of temperatures (2[degrees]C-25[degrees]C) that is likely to be encountered at typical vent habitats and in the water column above the vents (Epifanio et al. 1999). Effects of temperature on swimming rate were muted, with a [Q.sub.10] of 1.5 over the entire 23[degrees]C range of the experiments, compared with expected values of 2 to 3 over the tolerance range of a typical shallow water crab (Prosser 1973). We interpreted this eurythermal response to be an adaptation to larval dispersal in the cold water external to the vents, followed by settlement in the warm water at the vent sites.

Megalopae in our experiments also demonstrated active walking behavior over this same range of temperatures, and again the effect of temperature was muted with a [Q.sub.10] of 1.5. This behavior was unusual in that megalopa larvae generally walked laterally like adult crabs, rather than in an anterior/ posterior direction like the megalopae of shallow water crabs. Moreover, walking was the dominant form of locomotion at temperatures above 15[degrees], which is again unusual in comparison with the megalopae of shallow water species (Luckenbach & Orth 1992). This may be a special adaptation for vent existence in that megalopae would swim when in the cold waters of the surrounding water column, thus augmenting dispersal. However, once encountering the warm water at a vent, the larvae would settle and explore the vent community by walking before undergoing metamorphosis.

Taken as a whole, the results of these behavioral studies support the hypothesis that larval development in Bythograea thermydron occurs in the water column external to the vents. Results from the investigation show that the megalopa stage is physiologically capable of exploiting the entire water column from the cold bottom water surrounding the vent sites to the tropical surface waters above. However, the actual vertical distribution of the larval forms is unknown outside of a few collections of zoea and megalopa larvae from vent plumes or from open water near a vent site (see Epifanio et al. 1999). Nevertheless, and in contrast to preliminary speculation based on preserved specimens (Williams 1980), the megalopa stage of B. thermydron is an extremely good swimmer with speeds in warm water that are comparable to the fastest swimming megalopae of shallow water forms (Luckenbach & Orth 1992). Even at the temperatures typical of bottom water near the vents (2[degrees]C-5[degrees]C), the megalopa larvae are capable of sustained swimming at 4 cm [s.sup.-1], which is similar to the speed of tidal currents at this vent site and more than twice as great as the reported speed of subtidal bottom currents (Kim & Mullineaux 1998). Moreover, the propensity to swim increases significantly with decreasing temperature, so megalopae are likely to spend the majority of time swimming, as opposed to sitting on the bottom, when in the cold waters away from a vent site. Thus, if megalopae were to swim in the direction of a prevailing bottom current, their effective speed over bottom could be as great as 7 km [d.sup.-1] at ambient bottom temperatures, and even in still water their speed would be around 3.5 km [d.sup.-1].

At this point we know nothing about the duration of zoeal development or about the swimming behavior of zoeae. However, zoeal swimming in shallow water forms is only important in vertical migration, and horizontal transport is largely controlled by currents. Thus, long distance dispersal of B. thermydron may be effected by passive transport in ambient currents, whereas actual selection of settlement sites may be dependent on active swimming by megalopae. If we take the results of our laboratory data literally, megalopa larvae may be able to delay metamorphosis for several months until suitable settlement habitat is encountered. So, even if swimming in the natural environment were discontinuous (e.g., 8-12 h [d.sup.-l]), the larvae of B. thermydron could easily swim tens to hundreds of km in search of suitable vent sites during a megalopa stage that lasted 2 to 3 mo. The cues involved in fine-scale location of a vent or in induction of metamorphosis are unknown, but actual settlement at a site may be augmented by the inhibitory effect of high temperature on swimming.

Additional evidence that larval development in B. thermydron may occur higher in the water column away from the immediate vent environment comes from a study in our laboratory in which we compared stable isotope compositions of tissue from B. thermydron megalopae, juveniles, and adults (Dittel et al. 2005). Results of this investigation showed that the megalopal and first juvenile stages of B. thermydron had both carbon and nitrogen isotope signatures consonant with a phytoplankton source of primary production and similar to predatory crustaceans typical of deep sea environments extraneous to hydrothermal vents (e.g., Rau et al. 1982, Minagawa & Wada 1984, Saino & Hattori 1987). In contrast, later juvenile and adult stages of B. thermydron were isotopically similar to potential prey species like the tube worms, Paralvinella sp. and Riftia pachyptila (Jones 1980), which are obligate vent forms that are dependent on bacterially based chemosynthetic production. Similar trends in isotopic composition have been reported for various species of vent shrimp. For example, Gebruk et al. (2000) found that postlarval shrimp arrive at the vents carrying large organic reserves of photosynthetic origin. These reserves are subsequently diluted when the newly metamorphosed shrimp switch to chemosynthetically based diets available at the vent sites.

Our results were also coherent with earlier experimental studies that showed a significant effect of diet on the isotopic composition of juvenile stages of a shallow-water crab species, Callinectes sapidus (Dittel et al. 2000). In that earlier investigation, field-caught megalopae had isotope ratios that implied a phytoplankton-based food web. After 21 days under controlled dietary conditions, the blue crab megalopae had reached J-4, and their isotopic compositions had changed to reflect the respective diets in the different experimental treatments. Previous experimental work in our laboratory with B. thermydron had shown that newly metamorphosed juveniles require approximately 45 days to reach J-3 at temperatures comparable to those at the vent sites and an additional 40 d to reach J-4 (Epifanio et al. 1999). Thus, it appears that the juvenile B. thermydron had required about six weeks for their carbon isotope compositions to change from typical phytoplankton-based values to the bacteria-based values typical of endemic vent organisms.

Overall, these results imply that megalopal development occurs away from the vent sites and extraneous to the vent plume and that the growth of megalopae is supported by a food web based on phytoplankton in surface layer. However, once megalopae settle at a vent site, they undergo metamorphosis, and the Stage I juveniles become part of a bacteria-based food web at the vent. The isotope ratios of most other vent organisms that we sampled differed greatly from the [[delta].sup.13]C values of megalopae and Stage 1 juveniles--and this difference is too large to be explained by fractionation during a single trophic level transfer. Instead, [sup.13]C values of megalopae resemble those of particulate organic carbon and phytoplankton in the water column over the vents (Rau et al. 1982). For example, sedimenttrap material collected above an active vent site on the East Pacific Rise (11[degrees]N) had [sup.13]C values between -17.0 to -18.5[per thousand], intermediate between bivalve [sup.13]C-depleted tissue and [sup.13]Cenriched tissue of tube worms (Khripounoff & Alberic 1991). On the other hand, sediment-trap material sampled away from the vent had values ][delta].sup.13]C of -21 to -22[per thousand], indicative of a pelagic source of carbon. In addition, megalopae were considerably enriched in [[delta].sup.15]N compared with most vent species, further indicating that the source of nitrogen for vent crab larvae originates in the pelagic environment as well. The higher [[delta].sup.15]N values of the postlarvae are consistent with higher nitrogen values reported for deep sea waters in the eastern tropical Pacific Ocean (Saino & Hattori 1987).

Zoea larvae of B. thermydron have rarely been collected in the water column near the vents (Van Dover et al. 1984, Van Dover et al. 1985), and we were unable to obtain any free-swimming zoeae for isotope analysis in our investigation (Dittel et al. 2005). However, we were able to hold one ovigerous female crab under hyperbaric conditions until its eggs hatched. As expected, newly released zoeae larvae had [[delta].sup.13]C values (-12.2[per thousand]) that were similar to the female (-11.1[per thousand]) and to a number of other vent organisms but were clearly different from those of the megalopae. Because we were unsuccessful in culturing the zoea larvae, we were not able to conduct experiments to determine the effect of diet on isotopic composition. But if zoeal development occurs away from the vents (see later), we would anticipate that the isotopic composition of zoea larvae would eventually become similar to that observed in the megalopae.

Our results provide support for the hypothesis that larvae of the vent crab B. thermydron are neither retained at vent sites nor transported in the vent plume. There are a number of scenarios for the actual dispersal of the larvae (Fig. 4). For example, if larvae were to display a demersal pattern of behavior, they could be transported in bottom currents along the floor of the rift valley. Food sources for larvae transported in near-bottom currents might include benthopelagic amphipods, like H. hesmonectes, which are extremely abundant in the water column immediately above mussel beds and Riftia clumps (Shank et al. 1998, Sheader et al. 2000). However, these amphipod species, and H. hesmonectes in particular, have isotopic ratios typical of vent organisms like tube worms, limpets, and similar, and high concentrations of the amphipods are restricted to areas close to the vent site. Moreover, larvae transported by bottom currents within the rifts would also be under the influence of fallout from the plume (which also travels along the rift valley) and would be expected to have an isotopic composition that reflected the chemoautotrophic sources of production at the vents.

[FIGURE 4 OMITTED]

Another possibility is that larvae are dispersed at some height above the bottom, but external to the plume. Earlier work has shown that plankton biomass in this region of the water column is several times greater than that in the plume and consists of typical mesopelagic species, quite distinct from bentho-pelagic fauna associated with vent communities (Thomson et al. 1991, Burd & Thomson 1994, Burd et al. 1998). Although we did not measure the isotope ratios of plankton above the plume, earlier work has shown a clear dependence on production by surface phytoplankton (e.g., Pauly et al. 1998). Recently, Burd et al. (2002) reported that 513C values (-17 to -21[per thousand]) of particle feeders and predatory zooplankton in the epiplume are quite heavy and resemble those of some vent organisms. On the other hand, zooplankton farther away from the plume in the epipelagic and mesopelagic (bottom of photic zone to 1,000 m) zones had carbon isotope values that ranged between -19[per thousand] and -26.3[per thousand]. This is consistent with the isotopic composition of the megalopae and early juveniles in our stable isotope investigation (Fig. 4).

Overall, it appears that B. thermydron has a dispersal strategy similar to that hypothesized for several species of bresiliid shrimp indigenous to vents on the Mid-Atlantic Ridge. Studies of those species have reported larvae as much as 100 km from a known vent site and 1,000 m above the bottom and have concluded that dispersal generally occurs in mesopelagic regions extraneous to the vent environment (Pond et al. 1997, Pond et al. 2000a, Pond et al. 2000b, Herring & Dixon 1998) where the larvae rely on photosynthetically derived food sources (Copley et al. 1998, Gebruk et al. 2000). In B. thermydron this may be facilitated by the migration of ovigerous female crabs away from the immediate vicinity of a vent to peripheral areas wherein eggs are brooded and eventually hatched (Perovich et al. 2003). This behavior minimizes the chances of entrainment in the vent plume and may allow the migration of zoea larvae to a position higher in the water column without going through the plume. Because of the absence of more detailed information on currents in this region and on the duration of zoeal development, inference about the pattern of horizontal transport of these larvae is difficult. However, it is evident that recruitment to the vent community occurs during the megalopa stage and that megalopae possess a suite of behaviors that expedites settlement in the vent environment (Epifanio et al. 1999). The tissues of these newly settled megalopae have carbon and nitrogen isotope ratios that clearly reflect a planktonic existence supported by phytoplankton-based production. The isotopic composition of juvenile crabs implies a switch to a vent-based food web soon after settlement.

All things considered, our stable isotope study provided strong support for the hypothesis that B. thermydron megalopae depend on food sources that are part of a food web that originates with surface primary production--and that juvenile crabs switch to food sources that are part of the indigenous vent food web soon after metamorphosis (Dittel et al. 2005). One possible scenario is that zoeal and megalopal development occurs in the open water column, away from the vent sites and extraneous to the vent plume. This idea is supported by several lines of evidence: (1) the isotope data presented in this paper imply a phytoplankton-based food source for megalopae; (2) megalopae are tolerant of wide variations in temperature and hydrostatic pressure, which provides the physiological potential for existence in the water column away from vent sites (Epifanio et al. 1999); (3) brooding and hatching of eggs occurs on the periphery of vent sites where entrainment of pelagic larvae in the vent plume is unlikely (Kim et al. 1994, Mullineaux & France 1995, Perovich et al. 2003); and (4) the ontogeny of eye structure, beginning at hatching and continuing through J-1, is consonant with a switch from bathypelagic existence during larval stages to a benthic vent existence at metamorphosis (Jinks et al. 2002). As with all stable isotope data, our results are open to alternative interpretations. Our data provide strong support for the idea that megalopae and juveniles rely on different food sources. However, the measured isotopic composition of the megalopae collected in our study does not prove that megalopae depend on a food chain extraneous to the vent. A review of relevant literature (e.g., Van Dover & Fry 1989) yields the credible possibility that megalopae could selectively feed on certain vent species that would result in an isotopic composition similar to that measured here. Nevertheless, the surface-production hypothesis we present here is highly plausible, requires a minimum number of assumptions, and is supported by available biological (see earlier) and oceanographic evidence.

SUMMARY

The body of work reviewed in this paper describes a crab species that shares fundamental biological characteristics with typical shallow-water brachyurans, yet possesses a suite of highly evolved traits specific for life at hydrothermal vents. B. thermydron is one of only six known species of Bythograea and is very abundant at vent sites along the East Pacific Rise. Because of the large amount of scientific work at the EPR, almost everything we know about bythograeid vent crabs is based on studies of this single species.

The external morphology of juvenile and adult B. thermydron differs from shallow-water crabs in the lack of external pigmentation, the thin translucent carapace, and the lack of external eye structure. The unique eyes of adult B. thermydron are particularly interesting because the larval forms have typical brachyuran eye structure (although the retinal pigments are adapted for life at depths of 1,000 m or more) and because the naked retinas that serve as eyes in the adult stage are adapted for sensing the exceptionally dim light that is generated by the vents themselves.

Likewise, many aspects of the physiology of B. thermydron are explicitly adapted to the ambient vent environment. For example, juveniles and adults are unusually tolerant of conditions of low oxygen and high sulfides, and the oxygen-carrying capacity of hemocyanin in the blood of B. thermydron differs in important ways from that of shallow-water forms. Moreover, the megalopal, juvenile, and adult forms exhibit extreme thermal tolerance and are capable of functioning at temperatures ranging from 2[degrees]C at the vent periphery to 30[degrees]C near the vent orifice--all of this with little apparent need for acclimation. Lastly, whereas adults are unable to function at hydrostatic pressures below 65 atmospheres, the species nevertheless exhibits a tolerance for variation in pressure beyond that seen in other vent organisms, although the adaptive advantage of this tolerance is not at all clear.

Less is known about the reproductive biology of B. thermydron. Ovarian development is similar to that seen in shallow-water crabs, and like most shallow-water forms, there appears to be a seasonal cycle in the maturation of eggs. But again, the adaptive significance of this seasonality is not clear--and the environmental cues that control this seasonality are largely unknown as well. Mating has never been observed in the species, but the brooding of eggs appears to occur in the cold water at the vent periphery. There have been few observations of actual hatching, and these support the idea that larvae are released at the vent periphery and may not be entrained in the vent plume.

Larval development is similar to that in shallow-water crabs and consists of an undetermined number of zoeal stages followed by a single megalopa stage. Very few stage I zoeae have been collected in nature and advanced-stage zoeae have never been observed. Stage I zoeae differ from shallow-water forms in the arrangement and extraordinary number of spines and processes on the carapace, abdomen, and telson. Another distinguishing characteristic is the lack of asymmetry in the setation of the exopodites of the 1st maxillipeds of these larvae with respect of other brachyuran crabs. Megalopae are distinct in the crab-like shape of the carapace, their extremely large size (>8 mm carapace width), and in their bright red coloration. Megalopae are extremely eurythermal and are active swimmers that move at speeds comparable to the fastest swimming speeds reported for shallow-water forms.

Several lines of evidence support the hypothesis that zoeal development in B. thermydron occurs in the water column extraneous to the vent sites and that megalopae return to the sites when they are ready to settle and undergo metamorphosis. For example, the stable isotope data reviewed in this paper imply a phytoplankton-based food source for megalopae as compared with a chemosynthetically-based source for juveniles and adults living at the vents. In addition, the megalopal stage is tolerant of wide variation in temperature and hydrostatic pressure, which provides the physiological potential for existence in the water column away from vent sites. Furthermore, the brooding and hatching of eggs occurs on the periphery of vent sites where entrainment of pelagic larvae in the vent plume is unlikely. And finally, the ontogeny of eye structure, beginning at hatching and continuing through J-1, is consonant with a switch from bathypelagic existence during larval stages to a benthic vent existence at metamorphosis.

But as with most vent species, we know very little of the early life history of B. thermydron compared with relevant shallow-water forms. Hatching has been observed in the natural environment only a few times, and the female crabs were not collected during the event, so we can only assume that the crabs were in fact B. thermydron. Likewise, none of the stage I zoeae collected in the field were subjected to sophisticated taxonomic analysis, and the larvae released by ovigerous females in our laboratory appeared to have hatched in a premature state. Moreover, the advanced zoeal stages of B. thermydron have never been observed in the field or laboratory, and we can only guess at the typical number of stages based on the large size difference between megalopal specimens from the vent sites and newly hatched zoeal specimens from our laboratory.

In contrast to the difficulty in working with the zoeal form, the megalopal stage of B. thermydron is commonly collected at vent sites along the EPR, and work in our laboratory has shown these megalopae appear to behave normally and to survive long periods of time at atmospheric pressure. We know of no other vent species that provides such fertile ground for experimental studies on an early life history stage.

ACKNOWLEDGMENTS

The authors dedicate this paper to the memory of Melbourne R. Carriker, a long-time friend, mentor, and colleague. The authors also thank the captain and crew of the R/V Atlantis II and DSV Alvin group for assistance in collecting specimens. Much of the work reviewed here was supported by OCE-9618007 as part of the LARVE initiative of the National Science Foundation.

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ANA I. DITTEL, GINA PEROVICH ([dagger]) AND CHARLES E. EPIFANIO *

College of Marine and Earth Studies, University of Delaware, 700 Pilottown Road, Lewes, Delaware 19958

* Corresponding author. E-mail: epi@udel.edu

([dagger])Current Address: USEPA/ORD/NCER/8723F, 1200 Pennsylvania Ave., N.W., Washington, DC 20460.
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