Abstract
In situ growth rates were determined, using two, 1-yr mark/recapture experiments, conducted between September 1991 and July 1993, for an undescribed mytilid, Seep Mytilid Ia, at three hydrocarbon seep sites in the Gulf of Mexico. The sites are located at depths of 540 to 730m, approximately 27°45′N; 91°30′W, and are separated by distances of 6 to 18 miles. These seep mytilids harbor methanotrophic endosymbionts and use methane as both a carbon and energy source. The mussel habitats were chemically characterized by analysis of water samples taken from precisely located microenvironments over, among and below the mussels, using small-volume, interstitial water samplers and the “Johnson Sea Link” submersible. Substantial differences were found in habital conditions, growth rates, and population structure for the mussels at the three sites examined. The growth rate of these seep mytilids reflects the methane concentration in their immediate habitat. Mussels at sites with abundant methane had growth rates that were comparable to shallow water mytilids at similar temperatures (5 to 8°C) with increases in shell length up to 17 mm yr−1 documented for smaller mussels (<40 mm shell length). In conjunction with measurements of growth rates, three condition indices (glycogen content, tissue water content, and the ratio of ash-free dry weight to shell volume) were used to determine the relationship between the condition of the mussels, their growth rates, and their habitat chemistry. The three condition indices were correlated with growth rate and were often significantly different between mussels in different samples.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Arnold SF (1990) Mathematical statistics. Prentice Hall, Englewood Cliffs, NJ
Bayne BL (1976) Marine mussels, their ecology and physiology. Cambridge University Press, New York
Bayne BL, Widdows J, Moore MN, Salkild P, Worrall CM, Donkin P (1982) Some ecological consequences of the physiological and biochemical effects of petroleum compounds on marine molluscs. Phil Trans R Soc Lond (Ser B) 297:219–239
Bayne BL, Worrall CM (1980) Growth and production of mussels Mytilus edulis from two populations. Mar Ecol Prog Ser 3:317–328
Behrens EW (1988) Geology of a continental slope oil seep, Northern Gulf of Mexico, AAPG Bull-Am Ass Petrol G 72:105–114
Brooks JM, Cox HB, Bryant WR, Kennicutt MC II, Mann RG, McDonald TJ (1986) Association of gas hydrates and oil seepage in the Gulf of Mexico Org Geochem 10:221–234
Brooks JM, Kennicutt MC II, Fisher CR, Macko SA, Cole K, Cole K, Childress JJ, Bidigare RR, Vetter RD, (1987) Deep-sea hydrocarbon seep communities: evidence for energy and nutritional carbon sources. Science, NY 20:1138–1142
Brooks JM, Kennicutt MC II, MacDonald IR, Wilkinson DL, Guinasso NLJ, Bidigare RR, (1989) Gulf of Mexico hydrocarbon seep communities, Part IV. Descriptions of known chemosynthetic communities. Offshore Technol Conf 5954:663–667
Brooks JM, Wiesenburg DA, Roberts H, Carney RS MacDonald IR, Fisher CR, Guinasso NLJ, Sager WW, McDonald SJ, Burke RAJ, Aharon P, Bright TJ (1990) Salt, seeps and symbiosis in the Gulf of Mexico EOS Trans Am Geophys Un 71:1772–1773
Carney RS (1994) Consideration of the oasis analogy for chemosynthetic communities at Gulf of Mexico hydrocarbon vents. Geo-Mar Lett 14:149–159
Cary SC, Fisher CR, Felbeck H (1988) Mussel growth supported by methane as sole carbon and energy source. Science, NY 240:78–80
Childress JJ, Fisher CR (1992) The biology of hydrothermal vent animals: physiology, biochemistry and autotrophic symbiosis. Oceanogr mar Biol A Rev 30:337–441
Childress JJ, Fisher CR, Brooks JM, Kennicutt MC, Bidigare R, Anderson A (1986) A methanotrophic marine molluscan symbiosis: mussels fueled by gas. Science, NY 233:1306–1308
Clark AG, Keith LE (1988) Variation among extracted lines of Drosophila melanogaster in triacylglycerol and carbohydrate storage. Genetics 119:595–607
Corliss JB, Dymond J, Gordon LI, Edmond JM, Herzen RPV, Ballard RD, Green K, Williams D, Bainbridge A, Crane K, Andel THv (1979) Submarine thermal springs on the Galapagos Rift. Science, NY 203:1073–1083
Craeymeersch JA, Herman PMJ, Meire PM (1986) Secondary production of an intertidal mussel (Mytilus edulis L.) population in the Eastern Scheldt (S.W. Netherlands). Hydrobiologia 133:107–115
De Zwaan A, Mathieu M (1992) Cellular Biochemistry and Endocrinology. In: Gosling E (ed) The mussel Mytilus: ecology, physiology, genetics, and culture. Elsevier Science Publishers, Amsterdam, pp 223–308
Fisher CR (1990) Chemoautotrophic and methanotrophic symbioses in marine invertebrates. Rev aquat Sci 2:399–436
Fisher CR (1993) Oxidation of methane by deep-sea mytilids in the Gulf of Mexico. In: Oremland RS (ed) Biogeochemistry of global change: radiatively active trace gases. Chapman and Hall Inc., New York, pp 606–618
Fisher CR, Childress JJ, Arp AJ, Brooks JM, Distel D, Favuzzi JA, Felbeck H, Hessler R, Johnson KS, Kennicutt MC II, Maco SA, Newton A, Powell MA, Somero GN, Soto T (1988) Microhabitat variation in the hydrothermal vent mussel Bathymodiolus thermophilus, at Rose Garden vent on the Galapagos rift. Deep-Sea Res 35:1769–1792
Fisher CR, Childress JJ, Oremland RS, Bidigare RR (1987) The importance of methane and thiosulphate in the metabolism of the symbionts of two deep-sea mussels. Mar Biol 96:59–71
Fisher CR, Childress JJ, Sanders NK (1988) The role of vestimentiferan hemoglobin in providing an environment suitable for chemoautotrophic sulfide-oxidizing endosymbionts. Symbiosis 5:229–246
Forster GR (1981) A note on the growth of Arctica islandica. J mar biol Ass UK 61:817
Frenzel P, Thebrath B, Conrad R (1990) Oxidation of methane in the oxic surface layer of a deep lake sediment (Lake Constance). Fedn eur microbiol Soc (FEMS) Microbiol Ecol 73:149–158
Giboa-Garber N (1971) Direct spectrophotometric determination of inorganic sulfide in biological materials and in other complex mixtures. Analyt Biochem 43:129–133
Grassle JF, Sanders HL (1973) Life histories and the role of disturbance. Deep-Sea Res 20:643–659
Hessler RR, Smithey WM, Keller CH (1985) Spatial and temporal variation of giant clams, tubeworms and mussels at deep-sea hydrothermal vents. Bull biol Soc Wash 6:465–474
Hummel H, Wolf LD, Zurburg W, Apon L, Bogaards RH, Ruitenburg MV (1989) The glycogen content in stressed marine bivalves: the initial absence of a decrease. Comp Biochem Physiol 94B:729–733
Johnson KS, Childress JJ, Beehler CL (1988) Short term temperature variability in the Rose Garden hydrothermal vent field. Deep-Sea Res 35:1711–1722
Kennicutt MC II, Brooks JM, Bidigare RR, Denoux GJ (1988) Gulf of Mexico hydrocarbon seep communities — I. Regional distribution of hydrocarbon seepage and associated fauna. Deep-Sea Res 35:1639–1651
Kennicutt MC II, Brooks JM, Bidigare RR, Fay RR, Wade TL, McDonald TJ (1985) Vent-type taxa in a hydrocarbon seep region on the Louisiana Slope Nature, Lond 317:351–353
Keppler D, Decker K (1974) Glycogen determination with amyloglucosidase. In: Bergmeyer HU, Gawehn K (eds) Methods of enzymatic analysis, Vol 3. Academic Press, New York, pp 1127–1131
Kochevar R, Childress JJ, Fisher CR, Minnich E (1992) The methane mussel: roles of symbiont and host in the metabolic utilization of methane. Mar Biol 112:389–401
Kuivila KM, Murray JW, Devol AH, Lidstrom ME, Reimers CE (1988) Methane cycling in the sediments of Lake Washington. Limnol Oceanogr 33:571–578
Lilley MD, Baross JA, Gordon LI (1983) Reduced gases and bacteria in hydrothermal vent fluids: the Galapagos spreading center and 21°N East Pacific Rise. In: Rona PA, Bostrom K, Laubier L, Smith KL Jr. (ed) Hydrothermal processes at seafloor spreading centers Plenum Press, New York, pp 411–449
Lowe DM, Pipe RK (1986) Hydrocarbon exposure in mussels: a quantitative study of the responses in the reproductive and nutrient storage cell systems. Aquat Toxic 8:265–272
Lutz RA, Fritz LW, Rhoads DC (1985) Molluscan growth at deepsea hydrothermal vents. Bull biol Soc Wash 199–210
Lutz RA, Kennish MJ (1993) Ecology of deep-sea hydrothermal vent communities: a review. Rev Geophys 31:211–242
MacDonald IR, Best SE, Lee CS, Rost AA (1992) Biogeochemical processes at natural oil seeps in the Gulf of Mexico: field-trials of a small area imaging system (SABIS). Proceedings of the first thematic conference on remote sensing for marine and coastal environments, New Orleans, June 1992. Environmental Research Institute of Michigan, Ann Arbor, pp 261–272
MacDonald IR, Boland GS, Baker JS, Brooks JM, Kennicutt MC II, Bidigare RR (1989) Gulf of Mexico hydrocarbon seep communities. II. Spatial distribution of seep organisms and hydrocarbons at Bush Hill. Mar Biol 101:235–247
MacDonald IR, Guinasso NL, Reilly JF, Brooks JM, Callender WR, Gabrielle SG (1990a) Gulf of Mexico hydrocarbon seep communities. VI. Patterns in community structure and habitat. Geo-Mar Lett 10:244–252
MacDonald IR, Russell Callender W, Burke RA Jr., McDonald SJ, Carney RS (1990b) Fine-scale distribution of methanotrophic mussels at a Louisiana cold seep. Prog Oceanogr 24:15–24
McDonald SJ (1990) Benzo[a]pyrene metabolism in a deep sea mussel associated with natural petroleum seeps in the Gulf of Mexico. Dissertation. Texas A&M University, College Station
Merlivat L, Pineau F, Javoy M (1987) Hydrothermal vent waters at 13°N on the East Pacific Rise: isotopic composition and gas concentration. Earth planet Sci Lett 84:100–108
Neter J, Wasserman W, Kutner MH (1990) Applied linear statistical models. Irwin, Homewood, IL
Passonneau JV, Lauderdale VR (1974) A comparison of three methods of glycogen measurement in tissues. Analyt Biochem 60: 405–412
Powell MA, Somero GN (1986) Adaptations to sulfide by hydrothermal vent animals: sites and mechanisms of detoxification and metabolism. Biol Bull mar biol Lab, Woods Hole 171: 274–290
Raabo E, Terkildsen TC (1960) On the enzymatic determination of blood glucose. Scand J clin Lab Invest 12:402
Reiss MJ (1989) The allometry of growth and reproduction. Cambridge University Press, Cambridge
Rhoads DC, Lutz RA, Revelas EC, Cerrato RM (1981) Growth of bivalves at deep-sea hydrothermal vents along the Galapagos Rift. Science, NY 214:911–913
Roberts HH (1990) Sea floor responses to hydrocarbon seeps, Louisiana continental slope. Geo-Mar Lett 10:232–243
Seed R, Richardson CA (1990) Mytilus growth and its environmental responsiveness. In: Stefano GB (ed) Neurobiology of Mytilus edulis. Manchester University Press, Manchester, NY, pp 1–37
Seed R, Suchanek TH (1992) Population and community ecology of Mytilus. In: Gosling E (ed) The mussel Mytilus: ecology, physiology, genetics and culture. Elsevier Science Publishers, Amsterdam, pp 87–170
Smith KL Jr (1984) Deep-sea hydrothermal vent mussels: nutritional state and distribution at the Galapagos Rift. Ecology 66: 1067–1080
Stromgren T, Cary C (1984) Growth in length of Mytilus edulis L. fed on different algal diets. J exp mar Biol Ecol 76:23–34
Stromgren T, Nielsen MV (1991) Spawning frequency, growth, and mortality of Mytilus edulis larvae, exposed to copper and diesel oil. Aquat Toxic 21:171–180
Stromgren T, Nielsen MV, Ueland K (1986) Short-term effect of microencapsulated hydrocarbons on shell growth of Mytilus edulis. Mar Biol 91:33–39
Sukhotin AA, Kulakowski EE (1992) Growth and population dynamics in mussels (Mytilus edulis L.) cultured in the White Sea. Aquaculture, Amsterdam 101:59–73
Theisen BF (1973) The growth of Mytilus edulis L. (Bivalvia) from Disko and Thule District, Greenland. Ophelia 12:59–77
Thompson RJ (1984) Production, reproductive effort, reproductive value and reproductive cost in a population of the blue mussel Mytilus edulis in a subarctic environment. Mar Ecol Prog Ser 16: 249–257
Tunnicliffe V (1991) The biology of hydrothermal vents: ecology and evolution. Oceanog mar Biol A Rev 29:319–407
Turekian KK, Kharkar DP, Cerrato RM, Vaisnys JR, Sanders HL, Grassle JF, Allen JA (1975) Slow growth rate of a deep-sea clam determined by 228Ra chronology. Proc natl Acad Sci 72: 2829–2832
Wade TL, Kennicutt MC II, Brooks JM (1989) Gulf of Mexico hydrocarbon communities, III. Aromatic hydrocarbon concentrations in organisms, sediments, and water. Mar envirl Res 27: 19–30
Welhan JA, Craig H (1983) Methane, hydrogen, and helium in hydrothermal fluids at 21°N on the East Pacific Rise. In: Rona PA, Costrom K, Laubier L, Smith KLJ (eds) Hydrothermal processes at seafloor spreading centers. Plenum Press, New York, pp 391–409
Williams NA, Dixon DR, Southward EC, Holland PWH (1993) Molecular evolution and diversification of the vestimentiferan tube worms. J mar biol Ass UK 73:437–452
Wootton RJ (1991) Ecology of teleost fishes. Chapman & Hall, London
Author information
Authors and Affiliations
Additional information
Communicated by J.P. Grassle, New Brunswick
Rights and permissions
About this article
Cite this article
Nix, E.R., Fisher, C.R., Vodenichar, J. et al. Physiological ecology of a mussel with methanotrophic endosymbionts at three hydrocarbon seep sites in the Gulf of Mexico. Marine Biology 122, 605–617 (1995). https://doi.org/10.1007/BF00350682
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00350682