, Volume 161, Issue 2, pp 387–400 | Cite as

Imprint of past environmental regimes on structure and succession of a deep-sea hydrothermal vent community

  • Lauren S. Mullineaux
  • Fiorenza Micheli
  • Charles H. Peterson
  • Hunter S. Lenihan
  • Nilauro Markus
Community Ecology - Original paper


Dramatic perturbations of ecological communities through rapid shifts in environmental regime do not always result in complete mortality of residents. Instead, legacy individuals may remain and influence the succession and composition of subsequent communities. We used a reciprocal transplant experiment to investigate whether a legacy effect is detectable in communities experiencing an abrupt increase or decrease in hydrothermal fluid flux at deep-sea vents. Vent habitats are characterized by strong gradients in productivity and physico-chemical stressors, both of which tend to increase with increasing vent fluid flux. In our experiments, many species survived transplantation from cool (water temperatures <2°C above ambient) to warm (4–30°C above ambient) habitats, resulting in significantly higher species richness on transplanted than remaining experimental substrata. A legacy effect was much less apparent in transplantation from warm to cool habitat, although a few vestimentiferan tubeworms, normally restricted to warm habitat, survived transplantation. The asymmetry in influence of legacy individuals suggests that productivity enhancement may outweigh potential physiological stress in setting limits to distributions of vent invertebrates. This influence of biological processes contrasts with theory developed in the rocky intertidal that predicts the predominance of physical control at the high-stress end of an environmental gradient. Prediction of successional transitions in vents and other habitats experiencing regime shifts in which remnant species may survive must take into account the possible influence of historical effects.


Benthic community structure Vestimentiferan tubeworm East Pacific Rise Reciprocal transplant Legacy species 


  1. Arnett A, Gotelli N (1999) Geographic variation in life-history traits of the ant lion, Myrmeleon immaculatus: evolutionary implications of Bergmann’s rule. Evolution 53:1180–1188CrossRefGoogle Scholar
  2. Berlow E (1997) From canalization to contingency: historical effects in a successional rocky intertidal community. Ecol Monogr 67:435–460Google Scholar
  3. Butterfield D et al (1997) Seafloor eruptions and evolution of hydrothermal fluid chemistry. Philos Trans R Soc A 355:369–386CrossRefGoogle Scholar
  4. Chapman MG (1986) Assessment of some controls in experimental transplants of intertidal gastropods. J Exp Mar Biol Ecol 103:181–201CrossRefGoogle Scholar
  5. Childress JJ, Fisher CR (1992) The biology of hydrothermal vent animals: physiology, biochemistry, and autotrophic symbioses. Oceanogr Mar Biol 30:61–104Google Scholar
  6. Clements FE (1928) Plant succession and indicators. Wilson, New YorkGoogle Scholar
  7. Connell JH (1972) Community interactions on marine rocky intertidal shores. Annu Rev Ecol Syst 3:169–192CrossRefGoogle Scholar
  8. Connell JH (1975) Some mechanisms producing structure in natural communities: a model and some evidence from field experiments. In: Cody ML, Diamond JM (eds) Ecology and evolution of communities. Belknap, Cambridge, pp 460–490Google Scholar
  9. Connell JH, Slatyer RO (1977) Mechanisms of succession in natural communities and their role in community stability and organization. Am Nat 111:1119–1144CrossRefGoogle Scholar
  10. Connell JH, Hughes TP, Wallace CC (1997) A 30-year study of coral abundance, recruitment, and disturbance at several scales in space and time. Ecol Monogr 67:461–488Google Scholar
  11. D’Antonio CM, Hughes RF, Vitousek PM (2001) Factors influencing dynamics of invasive C4 grasses in a Hawaiian woodland: role of resource competition and priority effects. Ecology 82:89–104Google Scholar
  12. del Moral R (1983) Initial recovery of subalpine vegetation on Mount St. Helens, Washington. Am Midl Nat 109:72–80CrossRefGoogle Scholar
  13. Drury WH, Nisbet ICT (1973) Succession. J Arnold Arbor 54:331–368Google Scholar
  14. 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. In: Humphris SE, Zierenberg RA, Mullineaux LS, Thomson RE (eds) Seafloor hydrothermal systems: physical, chemical, biological, and geological interactions, vol Geophysical Monograph 91. American Geophysical Union, Washington, DC, pp 1–46Google Scholar
  15. Forrester GE, Fredericks BI, Gerdeman D, Evans B, Steele MA, Zayed K, Schweitzer LE, Suffet IH, Vance RR, Ambrose RF (2003) Growth of estuarine fish is associated with the combined concentration of sediment contaminants and shows no adaptation or acclimation to past conditions. Mar Environ Res 56:423–442PubMedCrossRefGoogle Scholar
  16. Franklin JF, Frenzen P, Swanson FJ (1988) Re-creation of ecosystems at Mt. St. Helens: contrasts in artificial and natural approaches. In: Cairns J Jr (ed) Rehabilitating damaged ecosystems, vol II. CRC, Boca Raton, pp 1–37Google Scholar
  17. Haymon RM, Fornari DJ, Edwards MH, Carbotte S, Wright W, 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
  18. Haymon RM, Fornari DJ, von Damm KL, Lilley MD, Perfit MR, Edmond JM, Shanks WC, 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 crest at 9°45–52′N: direct submersible observations of sea-floor phenomena associated with an eruption event in April, 1991. Earth Planet Sci Lett 119:85–101CrossRefGoogle Scholar
  19. 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 6:411–428Google Scholar
  20. Hessler RR, Smithey WM, Boudrias MA, Keller CH, Lutz RA, Childress JJ (1988) Temporal change in megafauna at the Rose Garden hydrothermal vent (Galápagos Rift; eastern tropical Pacific). Deep Sea Res 35:1681–1709CrossRefGoogle Scholar
  21. Hunt HL, Metaxas A, Jennings RM, Halanych K, Mullineaux LS (2004) Testing biological control of colonization by vestimentiferan tubeworms at deep-sea hydrothermal vents (East Pacific Rise, 9°50′N). Deep Sea Res I 51:225–234CrossRefGoogle Scholar
  22. Huston M, Smith T (1987) Plant succession: life history and competition. Am Nat 130:168–198CrossRefGoogle Scholar
  23. Jollivet D (1996) Specific and genetic diversity at deep-sea hydrothermal vents: an overview. Biodivers Conserv 5:1619–1653CrossRefGoogle Scholar
  24. Karl DM (1995) The microbiology of deep sea hydrothermal vents. CRC, New YorkGoogle Scholar
  25. Keeton WS, Franklin JF (2005) Do remnant old-growth trees accelerate rates of succession in mature Douglas-fir forests? Ecol Monogr 75:103–118CrossRefGoogle Scholar
  26. Le Bris N, Govenar B, Le Gall C, Fisher C (2006) Variability of physico-chemical conditions in 9°50′N EPR diffuse flow vent habitats. Mar Chem 98:167–182CrossRefGoogle Scholar
  27. Lee RW (2003) Thermal tolerances of deep-sea hydrothermal vent animals from the Northeast Pacific. Biol Bull 205:98–101PubMedCrossRefGoogle Scholar
  28. Lenihan HS, Mills SW, Mullineaux LS, Peterson CH, Fisher CR, Micheli F (2008) Biotic interactions at hydrothermal vents: recruitment inhibition by the mussel Bathymodiolus thermophilus. Deep Sea Res 55:1707–1717CrossRefGoogle Scholar
  29. Lubchenco J (1980) Algal zonation in the New England rocky intertidal community: an experimental analysis. Ecology 61:333–344CrossRefGoogle Scholar
  30. Lutz RA, Shank TM, Fornari DJ, Haymon RM, Lilley MD, Von Damm K, Desbruyères D (1994) Rapid growth at deep-sea vents. Nature 371:663–664CrossRefGoogle Scholar
  31. McCook LJ (1994) Understanding ecological community succession: causal models and theories, a review. Vegetatio 110:115–147CrossRefGoogle Scholar
  32. Micheli F, Peterson CH, Mullineaux LS, Fisher C, Mills SW, Sancho G, Johnson GA, Lenihan HS (2002) Predation structures communities at deep-sea hydrothermal vents. Ecol Monogr 72:338–365CrossRefGoogle Scholar
  33. Mills SW, Mullineaux LS, Tyler PA (2007) Habitat associations in gastropod species at East Pacific Rise hydrothermal vents (9°50′N). Biol Bull 212:185–194PubMedGoogle 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. Paine RT (1977) Controlled manipulations in the marine intertidal zone and their contributions to ecological theory. In: Goulden CE (ed) The changing scenes in natural sciences. Academy of Natural Sciences, Philadelphia, pp 245–270Google Scholar
  36. Platt WJ (1999) Southeastern pine savannas. In: Anderson RC, Fralish JS, Baskin JM (eds) Savannas, barrens, and rock outcrop plant communities of North America. Cambridge University Press, Cambridge, pp 23–51Google Scholar
  37. Platt WJ, Connell JH (2003) Natural disturbances and directional replacement of species. Ecol Monogr 73:507–522CrossRefGoogle Scholar
  38. 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
  39. Schoen DJ, Stewart SC, Lechowicz MJ, Bell G (1986) Partitioning the transplant site effect in reciprocal transplant experiments with Impatiens capensis and Impatiens pallida. Oecologia 70:149–154CrossRefGoogle Scholar
  40. Shank TM, Fornari DJ, von Damm KL, Lilley MD, Haymon RM, Lutz RA (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 45:465–515CrossRefGoogle Scholar
  41. Sousa W (2001) Natural disturbance and the dynamics of marine benthic communities. In: Bertness MD, Gaines SD, Hay ME (eds) Marine Community Ecology. Sinauer Associates, Sunderland, pp 85–130Google Scholar
  42. 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 314:1920–1922PubMedCrossRefGoogle Scholar
  43. Tunnicliffe V, McArthur AG, McHugh D (1998) A biogeographical perspective of the deep-sea hydrothermal vent fauna. Adv Mar Biol 34:355–442Google Scholar
  44. Underwood AJ, Denley EJ (1984) Paradigms, explanations and generalizations in models for the structure of intertidal communities on rocky shores. In: Strong DR, Simberloff D, Abele LG, Thistle AB (eds) Ecological communities: conceptual issues and the evidence. Princeton University Press, Princeton, pp 151–180Google Scholar
  45. von Damm KL (2000) Chemistry of hydrothermal vent fluids from 9°–10°N, East Pacific Rise: ‘‘Time zero’,’ the immediate posteruptive period. J Geophys Res Solid Earth 105:11203–11222CrossRefGoogle Scholar
  46. Wethey DS (1984) Sun and shade mediate competition in the barnacles Chthamalus and Semibalanus: a field experiment. Biol Bull 167:176–185CrossRefGoogle Scholar
  47. Wood DM, del Moral R (1987) Mechanisms of early primary succession in subalpine habitats on Mount St. Helens. Ecology 68:780–790CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Lauren S. Mullineaux
    • 1
  • Fiorenza Micheli
    • 2
  • Charles H. Peterson
    • 3
  • Hunter S. Lenihan
    • 4
  • Nilauro Markus
    • 5
  1. 1.Woods Hole Oceanographic InstitutionWoods HoleUSA
  2. 2.Stanford University, Hopkins Marine StationPacific GroveUSA
  3. 3.Institute of Marine SciencesUniversity of North Carolina at Chapel HillMorehead CityUSA
  4. 4.Bren School of Environmental Science and ManagementUniversity of CaliforniaSanta BarbaraUSA
  5. 5.Version3 IncSacramentoUSA

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