Marine Biology

, Volume 158, Issue 1, pp 181–192 | Cite as

Reproductive traits of pioneer gastropod species colonizing deep-sea hydrothermal vents after an eruption

  • S. R. Bayer
  • L. S. Mullineaux
  • R. G. Waller
  • A. R. Solow
Original Paper

Abstract

The colonization dynamics and life histories of pioneer species determine early succession at nascent hydrothermal vents, and their reproductive ecology may provide insight into their dispersal and population connectivity. Studies on the reproductive traits of two pioneer gastropod species, Ctenopelta porifera and Lepetodrilus tevnianus, began within a year after an eruption on the East Pacific Rise (EPR) that eliminated vent communities near 9°50′N from late 2005/early 2006. Standard histology was used to examine gamete release, instantaneous female fecundity, and time to maturation. Both species exhibited two-component oocyte size–frequency distributions indicating quasi-continuous reproduction with high fecundity. In samples collected in December 2006, both C. porifera and L. tevnianus individuals were reproductively mature. The smallest reproducing C. porifera were 4.2 mm (males) and 5.4 mm (females) in shell length, whereas reproductive L. tevnianus were smaller (2.3 and 2.4 mm in males and females, respectively). Most C. porifera were large (>6.0 mm) compared to their size at metamorphosis and reproductively mature. In contrast, most L. tevnianus were small (<1.0 mm) and immature. Reproductive traits of the two species are consistent with opportunistic colonization, but are also similar to those of other Lepetodrilus species and peltospirids at vents and do not fully explain why these particular species were the dominant pioneers. Their larvae were probably in high supply immediately after the eruption, due to oceanographic transport processes from remote source populations.

Supplementary material

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Supplementary material 1 (PDF 100 kb)
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Supplementary material 2 (PDF 167 kb)
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Supplementary material 3 (PDF 6814 kb)

References

  1. Adams DK (2007) Influence of hydrodynamics on the larval supply to hydrothermal vents on the East Pacific Rise. PhD thesis, Woods Hole Oceanographic InstitutionGoogle Scholar
  2. Adams DK, Mullineaux LS (2008) Supply of gastropod larvae to hydrothermal vents reflects transport from local larval sources. Limnol Oceanogr 53:1945–1955CrossRefGoogle Scholar
  3. Barrett SCH (1992) Genetics of weed invasions. In: Jain SK, Bostford LW (eds) Applied population biology. Kluwer Academic, Dordecht, pp 91–119CrossRefGoogle Scholar
  4. Berg CG (1985) Reproductive strategies of mollusks from abyssal hydrothermal vent communities. Biol Soc Wash Bull 6:185–197Google Scholar
  5. Bouchet P, Warén A (1994) Ontogenetic migration and dispersal of deep-sea gastropod larvae. In: Young CM, Eckelbarger KJ (eds) Reproduction, larval biology, and recruitment of the deep- sea benthos. Columbia University Press, New York, pp 98–117Google Scholar
  6. Butterfield D, Jonasson I, Massoth G, Feely R, Roe K, Embley R, Holden K, McDuff R, Lilley M, Delaney J (1997) Seafloor eruptions and evolution of hydrothermal fluid chemistry. Philos Trans R Soc Lond B Biol, Ser (A Math, Phys, Sci) 335:369–386CrossRefGoogle Scholar
  7. Chevaldonné P, Jollivet D, Vangriesheim A, Desbruyeres D (1997) Hydrothermal vent alvinellid polychaete dispersal in the eastern Pacific. 1. Influence of vent distribution, bottom currents, and biological patterns. Limnol Oceanogr 42:67–80CrossRefGoogle Scholar
  8. Cowen JP, Fornari DJ, Shank TM, Love B, Galzer B, Treusch A, Holmes RC, Soule SA, Baker ET, Tolstoy M, Pomranig KR (2007) Volcanic eruptions at East Pacific Rise near 9°50′N. Eos Trans Am Geophys Union 88:81–83CrossRefGoogle Scholar
  9. Eckelbarger KJ (1994) Diversity of metazoan ovary and vitellogenic mechanisms: implications for life history theory. Proc Biol Soc Wash 107:193–218Google Scholar
  10. Eckelbarger KJ, Watling L (1995) Role of phylogenetic constraints in determining reproductive patterns in deep-sea invertebrates. Invertebr Biol 114:256–269CrossRefGoogle Scholar
  11. Fornari DJ, Embley RW (1995) Tectonic and volcanic controls on hydrothermal processes at the mid-ocean ridge: an overview based on near-bottom and submersible studies. Geophys Monogr 91:1–46Google Scholar
  12. Fretter V (1988) New archaeogastropod gastropods from hydrothermal vents; superfamily Lepetodrilacea II. Anatomy. Philos Trans R Soc Lond B Biol Sci 319:33–82CrossRefGoogle Scholar
  13. Haymon RM, Fornari DJ, Edwards MH, Carbotte S, Wright D, Macdonald KC (1991) Hydrothermal vent distribution along the East Pacific Rise crest (9°09′–54′ N) and its relationship to magmatic and tectonic processes on fast-spreading mid-ocean ridges. Earth Planet Sci Lett 104:513–534CrossRefGoogle Scholar
  14. Haymon RM, Fornari DJ, Von Damm KL, Lilley MD, Perfit MR, Edmond JM, Shanks WC III, Lutz RA, Grebmeier JM, Carbotte S, Wright D, McLaughlin E, Smith M, Beedle N, Olson E (1993) Volcanic eruption of the mid-ocean ridge along the East Pacific Rise crew at 9°45–52′N: direct submersible observations of sea-floor phenomena associated with an eruption event April, 1991. Earth Planet Sci Lett 119:85–101CrossRefGoogle Scholar
  15. 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
  16. Johnson SB, Young CR, Jones WJ, Warén A, Vrijenhoek RC (2008) DNA barcoding of Lepetodrilus limpets reveals cryptic species. J Shell Res 27:43–51CrossRefGoogle Scholar
  17. Jollivet D (1996) Specific and genetic diversity at deep-sea hydrothermal vents: An overview. Bio divers Conserv 5:1619–1653Google Scholar
  18. Jollivet D, Chevaldonné P, Planque B (1999) Hydrothermal-vent alvinellid polychaete dispersal in the eastern Pacific. 2. A metapopulation model based on habitat shifts. Evolution 53:1128–1142CrossRefGoogle Scholar
  19. Karl DM (1995) The microbiology of deep sea hydrothermal vents. CRC, New YorkGoogle Scholar
  20. Kelly NE, Metaxas A (2007) Influence of habitat on the reproductive biology of the deep-sea hydrothermal vent gastropod Lepetodrilus fucensis (Vetigastropoda: Mollusca) from the Northeast Pacific. Mar Biol 151:649–662CrossRefGoogle Scholar
  21. Kiernan JA (2008) Histological and histochemical methods: theory and practice. Bloxham, United KingdomGoogle Scholar
  22. Kim SL, Mullineaux LS (1998) Distribution and near-bottom transport of larvae and other plankton at hydrothermal vents. Deep-Sea Res II 45:423–440CrossRefGoogle Scholar
  23. Levin LA (2006) Recent progress in understanding larval dispersal: new directions and digressions. Soc Integr Comp Biol 46:282–297CrossRefGoogle Scholar
  24. MacDonald KC, Becker K, Spiess FN, Ballard RD (1980) Hydrothermal heat flux of the “black smoker” vents on the East Pacific Rise. Earth Planet Sci Lett 48:1–7CrossRefGoogle Scholar
  25. Marsh AG, Mullineaux LS, Young CM, Manahan DT (2001) Larval dispersal potential of the tubeworm Riftia pachyptila at deep-sea hydrothermal vents. Nature 411:77–80CrossRefGoogle Scholar
  26. McHugh D, Tunnicliffe V (1994) Ecology and reproductive biology of the hydrothermal vent polychaete Amphisamytha galapagensis (Ampharetidae). Mar Ecol Prog Ser 106:111–120CrossRefGoogle Scholar
  27. McLachlan G (1987) On bootstrapping the likelihood ratio test statistic for the number of components in a normal mixture. Appl Stat 36:318–324CrossRefGoogle Scholar
  28. McLachlan G, Peel D (2000) Finite mixture models. Wiley-Interscience, New YorkCrossRefGoogle Scholar
  29. McLean JH (1988) New archaeogastropod limpets from hydrothermal vents; superfamily Lepetodrilacea I. Systematic descriptions. Philos Trans R Soc Lond B Biol Sci 319:1–32CrossRefGoogle Scholar
  30. McLean JH (1993) New species and record of Lepetodrilus (Vetigastropoda: Lepetodrilidae) from hydrothermal vents. Veliger 36:27–35Google Scholar
  31. Metaxas A (2004) Spatial and temporal patterns in larval supply at hydrothermal vents on the northeast Pacific Ocean. Limnol Oceanogr 49:1949–1956CrossRefGoogle Scholar
  32. Mills SW, Beaulieu SE, Mullineaux LS (2009) Photographic identification guide to larvae at hydrothermal vents. Woods Hole Oceanogr Inst Tech Rept WHOI-2009-05Google Scholar
  33. Mullineaux LS, Fisher CR, Peterson CH, Schaeffer SW (2000) Tubeworm succession at hydrothermal vents: use of biogenic cues to reduce habitat selection error? Oecologia 123:275–284CrossRefGoogle Scholar
  34. Mullineaux LS, Peterson CH, Micheli F, Mills SW (2003) Successional mechanism varies along a gradient in hydrothermal fluid flux at deep-sea vents. Ecol Monogr 73:523–542CrossRefGoogle Scholar
  35. Mullineaux LS, Mills SW, Sweetman AK, Beaudreau AH, Metaxas A, Hunt HL (2005) Vertical, lateral and temporal structure in larval distributions at hydrothermal vents. Mar Ecol Prog Ser 293:1–16CrossRefGoogle Scholar
  36. Mullineaux LS, Adams DK, Mills SW, Beaulieu SE (2010) Larvae from afar colonize deep-sea hydrothermal vents after a catastrophic eruption. Proc Natl Acad Sci 107:7829–7834CrossRefGoogle Scholar
  37. Neubert MG, Mullineaux LS, Hill MF (2006) A metapopulation approach to interpreting diversity at deep-sea hydrothermal vents. In: Kritzer JP, Sale PF (eds) Marine metapopulations. Elsevier Academic Press, Burlington, pp 321–352CrossRefGoogle Scholar
  38. Pendlebury SJD (2005) Ecology of hydrothermal vent gastropods. PhD thesis. School of Ocean and Earth sciences, SouthamptonGoogle Scholar
  39. Shank TM, Fornari DJ, Von Damm KL, Lilley MD, Haymon RM, Lutz R (1998) Temporal and spatial patterns of biological community development at nascent deep-sea hydrothermal vents (9°50′N, East Pacific Rise). Deep-Sea Res II 45:464–515CrossRefGoogle Scholar
  40. Soule SA, Fornari DJ, Perfit MR, Rubin K (2007) New insights into mid-ocean ridge volcanic processes from the 2005–2006 eruption of the East Pacific Rise, 9°46′N–9°56′N. Geology 35:1079–1082CrossRefGoogle Scholar
  41. Tolstoy M, Cowen JP, Baker ET, Fornari DJ, Rubin KH, Shank TM, Waldhauser F, Bohnenstiehl DR, Forsyth DW, Holmes RC, Love B, Perfit MR, Weekly RT, Soule SA, Glazer B (2006) A sea-floor spreading event captured by seismometers. Science 314:1920–1922CrossRefGoogle Scholar
  42. Tunnicliffe V (1992) The nature and origin of the modern hydrothermal vent fauna. Palaios 7:338–350CrossRefGoogle Scholar
  43. Tyler PA, Young CM (1999) Reproduction and dispersal at vents and cold seeps. J Mar Biol Ass UK 79:193–208CrossRefGoogle Scholar
  44. Tyler PA, Campos-Creasey LS, Giles LA (1994) Environmental control of quasi-continuous and seasonal reproduction in deep-sea benthic invertebrates. In: Young CM, Eckelbarger KJ (eds) Reproduction, larval biology and recruitment of the Deep-Sea Benthos. Columbia University Press, New York, pp 158–178Google Scholar
  45. Tyler PA, Pendlebury S, Mills SW, Mullineaux LS, Eckelbarger KJ, Baker M, Young CM (2008) Reproduction of gastropods from vents on the East Pacific Rise and the Mid-Atlantic Ridge. J Shellfish Res 27:107–118CrossRefGoogle Scholar
  46. Van Dover CL (2000) The ecology of deep-sea hydrothermal vents. Princeton University Press, PrincetonGoogle Scholar
  47. Van Dover CL, Factor JR, Williams AB, Berg CJ (1985) Reproductive patterns of decapod crustaceans from hydrothermal vents. Biol Soc Wash Bull 6:223–227Google Scholar
  48. Von Damm KL (1990) Seafloor hydrothermal activity: black smoker chemistry and chimneys. Annu Rev Earth Planet Sci 18:173–204Google Scholar
  49. Von Damm KL (1995) Controls on the chemistry and temporal variability of seafloor hydrothermal fluids. In: Humphris SE, Zierenberg RA, Mullineaux LS, Thornson RE (eds) Seafloor hydrothermal systems: physical, chemical, biological, and geological interactions. Am Geophys Union, Washington, DC, pp 222–247Google Scholar
  50. Von Damm KL, Bates MJ, Carmichael SK, Meana-Prado F, McDermott JM (2006) Response of the 9-10 N EPR hydrothermal systems to recent volcanic eruptions, Eos Trans Am Geophys Union, 87, Fall Meet Suppl, Abstract V13C-02Google Scholar
  51. Vrijenhoek RC (1997) Gene flow and genetic diversity in naturally fragmented metapopulations of deep-sea hydrothermal vent animals. J Hered 88:285–293Google Scholar
  52. Warén A, Bouchet P (1993) New records, species, genera and a new family of gastropods from hydrothermal vents and hydrocarbon seeps. Zool Scrip 22:1–90CrossRefGoogle Scholar
  53. Watremez P, Kervevan C (1990) Origine des variations de l’activité hydrothermale: premiers éléments de réponse d’un modèle numérique simple. C R Acad Sci Paris, Ser II 311:153–158Google Scholar
  54. Young CM (2003) Reproduction, development and life-history traits. In: Tyler PA (ed) Ecosystems of the deep oceans. Elsevier, Amsterdam, pp 381–426Google Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • S. R. Bayer
    • 1
  • L. S. Mullineaux
    • 1
  • R. G. Waller
    • 2
  • A. R. Solow
    • 3
  1. 1.MS 34, Biology DepartmentWoods Hole Oceanographic InstitutionWoods HoleUSA
  2. 2.School of Ocean and Earth Sciences and TechnologyUniversity of Hawaii at ManoaHonoluluUSA
  3. 3.Marine Policy CenterWoods Hole Oceanographic InstitutionWoods HoleUSA

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