Marine Biology

, Volume 152, Issue 3, pp 557–568 | Cite as

Persistence, morphology, and nutritional state of a gastropod hosted bacterial symbiosis in different levels of hydrothermal vent flux

  • Amanda E. BatesEmail author
Research Article


The limpet, Lepetodrilus fucensis McLean, is found in prominent stacks around hydrothermal vents on the Juan de Fuca Ridge. L. fucensis hosts a filamentous episymbiont on its gill lamellae that may be ingested directly by the gill epithelium. To assess the persistence of this symbiosis I used microscopy to examine the gills of L. fucensis from sites representing its geographic range and different habitats. The symbiosis is present on all the specimens examined in this study, including both sexes and a range of juvenile and adult sizes. Next, I aimed to determine if patterns in bacterial abundance, host condition, and gill morphology support the hypotheses that the bacteria are chemoautotrophic and provide limpets with a food resource. To do so, I compared specimens from high and low flux locations at multiple vents. My results support the above hypotheses: (1) gill bacteria are significantly less abundant in low flux where the concentrations of reduced chemicals (for chemoautotrophy) are negligible, (2) low flux specimens have remarkably poor tissue condition, and (3) the lamellae of high flux limpets have greater surface area: the blood space and bacteria-hosting epithelium are deeper and have more folds than low flux lamellae, modifications that support higher symbiont abundances. I next asked if the morphology of the lamellae could change. To test this, I moved high flux limpets away from a vent and after 1 year the lamellar depth and shape of the transplanted specimens resembled low flux gills. Last, I was interested in whether bacterial digestion by the gill epithelium is a significant feeding mechanism. As bacteria-like cells are rarely apparent in lysosomes of the gill epithelium, I predicted that lysosome number would be unrelated to bacterial abundance. My data support this prediction, suggesting that digestion of bacteria by the gill epithelium probably contributes only minimally to the limpet’s nutrition. Overall, the persistence and morphology of the L. fucensis gill symbiosis relates to the intensity of vent flux and indicates that specimens from a variety of habitats may be necessary to characterize the morphological variability of gill-hosted symbioses in other molluscs.


Shell Length Bacterial Abundance Gill Epithelium Gill Lamella Flux Location 
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V. Tunnicliffe provided samples, financial support, and comments on the manuscript. R. Campbell performed the lipid analyses. Technical support from the ROPOS team and the crew of the RV Thompson is especially appreciated. Research cruise scientists, in particular S. K. Juniper, made this work possible. Special effort by B. Embley, J. Delaney, and D. Kelly was made to recover samples and the experiment during rough weather. T. Bird, R. Campbell, L. Page, J. Rose, and C.L. Singla provided technical support. NSERC Canada, the NOAA Vents Program, and graduate student scholarships to A. Bates from NSERC Canada and the families of Gordon Fields and Maureen de Burgh provided funding for this study.


  1. Anthony KRN, Hoogenboom MO, Connolly SR (2005) Adaptive variation in coral geometry and the optimization of internal colony light climates. Funct Ecol 19:17–26CrossRefGoogle Scholar
  2. Bates AE (2006) Population and feeding characteristics of hydrothermal vent gastropods along environmental gradients with a focus on a bacterial symbiosis hosted by Lepetodrilus fucensis (Vetigastropoda). PhD Thesis, Department of Biology, University of VictoriaGoogle Scholar
  3. Bates AE, Tunnicliffe V, Lee RW (2005) Role of thermal conditions in habitat selection by hydrothermal vent gastropods. Mar Ecol Prog Ser 305:1–15CrossRefGoogle Scholar
  4. Boetius A, Felbeck H (1995) Digestive enzymes in marine-invertebrates from hydrothermal vents and other reducing environments. Mar Biol 122:105–113CrossRefGoogle Scholar
  5. Campbell RW, Boutillier P, Dower JF (2004) Ecophysiology of overwintering in the copepod Neocalanus plumchrus: changes in lipid and protein contents over a seasonal cycle. Mar Ecol Prog Ser 280:211–226CrossRefGoogle Scholar
  6. de Burgh ME (1986) Evidence for a physiological gradient in the vestimentiferan trophosome: size-frequency analysis of bacterial populations and trophosome chemistry. Can J Zool 64:1095–1103CrossRefGoogle Scholar
  7. de Burgh ME, Singla CL (1984) Bacterial colonization and endocytosis on the gill of a new limpet species from a hydrothermal vent. Mar Biol 84:1–6CrossRefGoogle Scholar
  8. DeChaine EG, Bates AE, Shank TM, Cavanaugh CM (2006) Off-axis symbiosis found: characterization and biogeography of bacterial symbionts of Bathymodiolus mussels from Lost City hydrothermal vents. Environ Microbiol 8(11):1902–1912CrossRefGoogle Scholar
  9. Distel D, Felbeck H (1988) Pathways of inorganic carbon fixation in the endosymbiont-bearing lucinid clam Lucinoma aequizonata. II. Analysis of the individual contributions of host and symbiont to organic carbon assimilation. J Exp Zool 247:11–22CrossRefGoogle Scholar
  10. Dubilier N, Mulders C, Ferdelman T, de Beer D, Pernthaler A, Klein M, Wagner M, Erseus C, Thiermann F, Krieger J, Giere O, Amann R (2001) Endosymbiotic sulphate-reducing and sulphide-oxidizing bacteria in an oligochaete worm. Nature 411:298–302CrossRefGoogle Scholar
  11. Fisher CR (1990) Chemoautotrophic and methanotrophic symbioses in marine invertebrates. Crit Rev Aquat Sci 2:399–436Google Scholar
  12. Fisher CR, Childress JJ (1986) Translocation of fixed carbon from symbiotic bacteria to host tissues in the gutless bivalve Solemya reidi. Mar Biol 93:59–68CrossRefGoogle Scholar
  13. Flores JF, Fisher CR, Carney SL, Green BN, Freytag JK, Schaeffer SW, Royer WE (2005) Sulfide binding is mediated by zinc ions discovered in the crystal structure of a hydrothermal vent tubeworm hemoglobin. Proc Natl Acad Sci USA 102:2713–2718CrossRefGoogle Scholar
  14. Fox M, Juniper SK, Vali H (2002) Chemoautotrophy as a possible nutritional source in the hydrothermal vent limpet Lepetodrilus fucensis. Cah Biol Mar 43:371–376Google Scholar
  15. Fretter V (1988) New archaeogastropod limpets from hydrothermal vents; Superfamily Lepetodrilacea II. In: Cann JR, Elderfield H, Laughton A (eds) Mid-Ocean Ridges: dynamics of processes associated with creation of new ocean crust. Phil Trans Roy Soc Lon B, vol 309(1192), pp 33–82Google Scholar
  16. Goffredi SK, Warén A, Orphan VJ, Dover CLV, Vrijenhoek RC (2004) Novel forms of structural integration between microbes and a hydrothermal vent gastropod from the Indian Ocean. Appl Environ Microbiol 70:3082–3090CrossRefGoogle Scholar
  17. Gros O, Frenkiel L, Moueza M (1998) Gill filament differentiation and experimental colonization by symbiotic bacteria in aposymbiotic juveniles of Codakia orbicularis (Bivalvia: Lucinidae). Invertebr Reprod Dev 34:219–231CrossRefGoogle Scholar
  18. Hourdez S, Jouin-Toulmond C (1998) Functional anatomy of the respiratory system of Branchipolynoe species (Polychaeta, Polynoidae), commensal with Bathymodiolus species (Bivalvia, Mytilidae) from deep-sea hydrothermal vents. Zoomorphology 118:225–233CrossRefGoogle Scholar
  19. Johnson KS, Beehler CL, Sakamoto-Arnold CM, Childress JJ (1986) In situ measurements of chemical distributions in a deep-sea hydrothermal vent field. Science 231:1139–1141CrossRefGoogle Scholar
  20. Kadar E, Bettencourt R, Costa V, Santos RS, Lobo-Da-Cunha A, Dando P (2005) Experimentally induced endosymbiont loss and re-acquirement in the hydrothermal vent bivalve Bathymodiolus azoricus. J Exp Mar Biol Ecol 318: 99–110CrossRefGoogle Scholar
  21. Manly B (1991) Randomization and Monte Carlo methods in biology. Chapman and Hall, LondonCrossRefGoogle Scholar
  22. Minic Z, Gaill F, Herve G (2002) Metabolism of pyrimidine nucleotides in the deep-sea tubeworm Rifita pachytila and its bacterial endosymbiont. Cah Biol Mar 43:351–354Google Scholar
  23. Muller-Parker G, Davy SK (2001) Temperate and tropical algal-sea anemone symbioses. Invertebr Biol 120:104–123CrossRefGoogle Scholar
  24. Raulfs E, Macko S, Van Dover CL (2004) Tissue and symbiont condition of mussels (Bathymodiolus thermophilus) exposed to varying levels of hydrothermal activity. J Mar Biol Assoc UK 84:229–234CrossRefGoogle Scholar
  25. Sarrazin J, Juniper SK, Massoth G, Legendre P (1999) Physical and chemical factors influencing species distributions on hydrothermal sulfide edifices of the Juan de Fuca Ridge, northeast Pacific. Mar Ecol Prog Ser 190:89–112CrossRefGoogle Scholar
  26. Smith KL (1985) Deep-sea hydrothermal vent mussels: nutritional state and distribution at the Galapagos Rift. Ecology 66:1067–1080CrossRefGoogle Scholar
  27. Tsurumi M, Tunnicliffe V (2003) Tubeworm-associated communities at hydrothermal vents on the Juan de Fuca Ridge, northeast Pacific. Deep-Sea Res I 50:611–629CrossRefGoogle Scholar
  28. Urakawa H, Dubilier N, Fujiwara Y, Cunningham DE, Kojima S, Stahl DA (2005) Hydrothermal vent gastropods from the same family (Provannidae) harbor phylogenetically distant gamma- and epsilon-proteobacterial endosymbionts. Environ Microbiol 7:750–754 CrossRefGoogle Scholar
  29. Urcuyo IA, Massoth GJ, Julian D, Fisher CR (2003) Habitat, growth and physiological ecology of a basaltic community of Ridgeia piscesae from the Juan de Fuca Ridge. Deep-Sea Res I 50:763–780CrossRefGoogle Scholar
  30. West SA, Kiers TE, Pen I, Denison RF (2002) Sanctions and mutualism stability: when should less beneficial mutualists be tolerated? J Evol Biol 15:830–837CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  1. 1.Department of BiologyUniversity of VictoriaVictoriaCanada

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