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Bathymodiolus Childressi) from a Bathyal, Methane Seep Environment (Northern Gulf of Mexico), Marine Biology 135: 635‐646 Doi: 10.1007/S002270050664

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Bathymodiolus Childressi) from a Bathyal, Methane Seep Environment (Northern Gulf of Mexico), Marine Biology 135: 635‐646 Doi: 10.1007/S002270050664 FAU Institutional Repository http://purl.fcla.edu/fau/fauir This paper was submitted by the faculty of FAU’s Harbor Branch Oceanographic Institute Notice: ©1999 Springer‐Verlag. This manuscript is a version of an article with the final publication found online at http://www.springerlink.com and may be cited as: Eckelbarger, K. J. and C. M. Young (1999) Ultrastructure of gametogenesis in a chemosynthetic mytilid bivalve (Bathymodiolus childressi) from a bathyal, methane seep environment (northern Gulf of Mexico), Marine Biology 135: 635‐646 doi: 10.1007/s002270050664 Marine Biology (1999) 135: 635±646 Ó Springer-Verlag 1999 K. J. Eckelbarger á C. M. Young Ultrastructure of gametogenesis in a chemosynthetic mytilid bivalve (Bathymodiolus childressi ) from a bathyal, methane seep environment (northern Gulf of Mexico) Received: 24 May 1999 / Accepted: 10 September 1999 Abstract The ultrastructural features of gametogenesis methane seep environment and presumed continuous have been described in the methane-seep mytilid bivalve availability of nutrients, reproduction parallels that of Bathymodiolus childressi Gustafson, Turner, Lutz & littoral mytilids, suggesting some phylogenetic con- Vrijenhoek, 1998 collected from the Gulf of Mexico in straints on the capacity for variability in gametogenic August 1995. This is the ®rst ultrastructural description processes in the family Mytilidae. of gametogenesis in any methane-seep bivalve. B. chil- dressi is gonochoric, and both the testis and ovary consist of acini surrounded by inter-acinal tissue com- posed of adipogranular cells that serve a nutrient storage Introduction function. Oocytes develop in close association with squamous follicle cells although the follicle cells do not Dense macrofaunal communities of vestimentiferan appear to play a primary role in yolk synthesis. During tubeworms and modioliform mussels (Mytilidae) are the vitellogenic phase, biosynthesis of four types of or- associated with sites of oil and methane seepage at ganelles occurs, including lipid droplets, yolk granules, depths >500 m on the Louisiana slope of the Gulf of cortical granules, and unknown inclusions, which are Mexico (Kennicutt et al. 1985). The mussels attain a exocytosed as part of egg envelope biogenesis. Vitello- high biomass around these hydrocarbon seeps and har- genesis appears to be largely autosynthetic involving the bor methanotrophic endosymbionts in their gills. The Golgi complex and rough endoplasmic reticulum. Sperm bacterial symbionts oxidize methane and reduced car- dierentiation resembles that reported in other mytilid bon although the mussels also derive nutrition from bivalves and includes the dierentiation of proacroso- other sources, including ®lter feeding (reviewed by Lee mal granules and a ¯agellum during the early stages of et al. 1992; Lee and Childress 1995, 1996). Despite the spermatogenesis. Mature sperm have a cap-like acro- intense interest in the nutritional biology and physiology some, substantial subacrosomal material, a bullet- of hydrothermal vent and seep-associated mussels, very shaped nucleus, and four to ®ve mitochondria in the little information is available on reproduction (reviewed midpiece. The general features of gametogenesis closely by Tunniclie 1991; Mullineaux and France 1995; Tyler resemble those reported in shallow-water, seasonally and Young 1999). There is limited ultrastructural in- reproducing mytilids. Despite the relatively stable formation on the sperm, eggs, interstitial tissue, and gonoducts of an unidenti®ed species of Bathymodiolus from the East Paci®c Rise (Herry and Le Pennec 1987), Communicated by J.P. Grassle, New Brunswick and, more recently, Le Pennec and Beninger (1997) de- K.J. Eckelbarger (&) scribed features of spermatogenesis and mature sperm Darling Marine Center, University of Maine, 193 Clark's Cove Rd., Walpole, Maine 04573, USA ultrastructure in three species of Bathymodiolus from the East Paci®c Rise, the mid-Atlantic ridge, and the North e-mail: [email protected]; Fiji Basin. There are anecdotal observations on repro- Fax: +1-207-5633119 duction of deep-sea mytilids (Berg 1985; Hessler et al. K.J. Eckelbarger 1988) for B. thermophilus in the eastern Paci®c, and for School of Marine Sciences, University of Maine, Libby Hall, Orono, Maine 004469, USA an undescribed species of Bathymodiolus from the Lucky Strike vent ®eld on the Mid-Atlantic Ridge (Comtet and C.M. Young Á Division of Marine Sciences, Desbruyeres 1998). Harbor Branch Oceanographic Institution, There are no ultrastructural descriptions of the go- 5600 U.S. 1 North, Ft. Pierce, Florida 34946, USA nads or gametogenesis for mussels from methane seep 636 sites, and only limited information on deep-sea mussels, c in general. Hydrothermal vents and cold-water methane Fig. 1a±f Bathymodiolus childressi. a Light microscopic transverse seeps are created by dierent geological processes, and section through the ovary showing developing oocytes within acini. Note oocytes in early (1), middle (2), and late (3) stages of the lack of species overlap between these distinct com- vitellogenesis. Arrowheads indicate stalk-like connection of oocyte munities suggests some fundamental ecological dier- to ovary wall (N nucleus). Scale bar 40 lm. b Adipogranular ences (Tunniclie 1991). Hydrothermal vents are (ADG) cell showing lipid droplets (L), electron dense granules (*), and unpredictable and ephemeral, which implies that species glycogen (GL). Scale bar 10 lm. c Higher magni®cation of ADG living there might undergo rapid growth and reproduc- cells showing lipid (L), electron dense granules (*), and glycogen (GL). Scale bar 1.0 lm. d Previtellogenic oocyte (OC) in close association tion (Craddock et al. 1995). In contrast, methane seep with follicle cell containing extensive arrays of rough endoplasmic sites are believed to be more stable and to provide a reticulum (RER) (N nucleus; Nu nucleolus; M mitochondrion). Scale more constant source of nutrients. This suggests that bar 2.0 lm. e Follicle cell containing nucleus (N), mitochondrion selective pressures on species in these two contrasting (M), rough endoplasmic reticulum (RER), and lysosomal-like inclusion (*). Scale bar 2.0 lm. f Nuage-like granules in ooplasm habitats might result in divergent life history patterns, of previtellogenic oocyte. Scale bar 2.0 lm including dierences in reproductive seasonality. Bathymodiolus thermophilus was the ®rst hydrother- mal vent mussel described (Kenk and Wilson 1985), and (MacDonald et al. 1990) at 710 m depth (27°43.327¢N; at least seven additional species are now recognized from 91°16.606¢W). For ultrastructural studies, fresh gonadal tissues from male and female specimens of varying sizes were selected for vent sites (reviewed by Gustafson et al. 1998). Craddock ®xation: three females with maximum shell lengths (SL) of 83, 96, et al. (1995) identi®ed several additional modioliform and 110 mm and three males with SL of 70, 92, and 105 mm. taxa from sul®de/hydrocarbon seeps in the Gulf of Me- Tissue samples were excised and immersed for 1.5 h in cold (4 °C) xico using an allozyme survey and, recently, Gustafson primary ®xative containing 3% glutaraldehyde, 1% formaldehyde made from paraformaldehyde, 0.1 M Millonig's phosphate buer et al. (1998) described ®ve mussel species from this sur- (pH 7.4), 3% NaCl, and 3.5% sucrose. Tissue was then rinsed for vey. Prior to the work of Craddock et al. (1995), seep and 30 min in three changes of cold (4 °C) 0.1 M Millonig's phosphate hydrothermal vent mytilids were assumed to be closely buer containing 6% sucrose. The tissue was then post®xed for related but it now appears that there are no mytilid 1.5 h at room temperature in 1% OsO4 in 0.1 M Millonig's phos- species common to both habitats. In the present study, phate buer and dehydrated for 2 h in ascending concentrations of ethanol. The ®nal dehydrations with 100% ethanol and with two we describe the ultrastructural features of the gonad and changes of propylene oxide (2 min each) were followed by em- gametogenesis in the well-studied methane seep species bedding in Epon. Thin sections were cut with a diamond knife on a Bathymodiolus childressi, which has recently been de- Porter-Blum MT2-B ultramicrotome, stained with uranyl acetate scribed (Gustafson et al. 1998). This species has been followed by lead citrate, and examined with a Zeiss EM 10-A transmission electron microscope (TEM). referred to in the literature by various names since 1985, including Seep Mytilid 1a (Louisiana Continent Slope) and Seep Mytilid 1b (Alaminos Canyon) (reviewed by Gustafson et al. 1998). Placement of this species in the Results genus Bathymodiolus is provisional pending a more complete morphological and molecular analysis (R. Lutz General morphology of the gonad personal communication). The ®ne-scale distribution of this species on the Louisiana slope is correlated with Bathymodiolus childressi is a gonochoric species, and we methane concentration (MacDonald et al. 1989), and saw no histological evidence of hermaphroditism. We dense populations are found around brine-®lled depres- saw no signi®cant dierence in degree of gamete devel- sions on the ocean ¯oor where brine density reaches 3.5 opment in either sex in the specimens we sampled, and times that of normal seawater (MacDonald et al. 1990a, none of the specimens were immature. The gonad is a b). The species has been recorded from a maximum depth simple structure consisting of acini surrounded by inter- of 2222 m at Alaminos Canyon in the western Gulf of acinal tissue composed of adipogranular cells. Each Mexico (Gustafson et al. 1998). Preliminary data from acinus contains developing germ cells and is bathed ex- histological sections of the gonads and analysis of pop- ternally in hemal ¯uid contained within an anastomos- ulation structure (M. Baker, P. Tyler and C. Young ing hemocoelic space. In the ovary, developing oocytes unpublished) indicate that this species reproduces sea- are also associated with follicle cells. In transverse sec- sonally, and that its recruitment is intermittent. The tion, each acinus contains peripherally arranged germ present study is the ®rst to document gametogenesis in cells surrounding a central lumen.
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