Extreme longevity in a deep-sea vestimentiferan tubeworm and its implications for the evolution of life history strategies (original) (raw)

Abstract

The deep sea is home to many species that have longer life spans than their shallow-water counterparts. This trend is primarily related to the decline in metabolic rates with temperature as depth increases. However, at bathyal depths, the cold-seep vestimentiferan tubeworm species Lamellibrachia luymesi and Seepiophila jonesi reach extremely old ages beyond what is predicted by the simple scaling of life span with body size and temperature. Here, we use individual-based models based on in situ growth rates to show that another species of cold-seep tubeworm found in the Gulf of Mexico, Escarpia laminata, also has an extraordinarily long life span, regularly achieving ages of 100–200 years with some individuals older than 300 years. The distribution of results from individual simulations as well as whole population simulations involving mortality and recruitment rates support these age estimates. The low 0.67% mortality rate measurements from collected populations of E. laminata are similar to mortality rates in L. luymesi and S. jonesi and play a role in evolution of the long life span of cold-seep tubeworms. These results support longevity theory, which states that in the absence of extrinsic mortality threats, natural selection will select for individuals that senesce slower and reproduce continually into their old age.

Access this article

Log in via an institution

Subscribe and save

• Get 10 units per month
• Download Article/Chapter or eBook
• 1 Unit = 1 Article or 1 Chapter
• Cancel anytime Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

• Andrews A, Cordes E, Mahoney M (2002) Age, growth and radiometric age validation of a deep-sea, habitat-forming gorgonian (Primnoa resedaeformis) from the Gulf of Alaska. Hydrobiologia 101–110
• Atanasov AT (2005) The linear alometric relationship between total metabolic energy per life span and body mass of poikilothermic animals. Biosystems 82:137–142. doi:10.1016/j.biosystems.2005.06.006
  Article PubMed Google Scholar
• Austad SN (1993) Retarded senescence in an insular population of Virginia opossums (Didelphis virginiana). J Zool 229:695–708. doi:10.1111/j.1469-7998.1993.tb02665.x
  Article Google Scholar
• Becker EL, Cordes EE, Macko SA et al (2013) Using stable isotope compositions of animal tissues to infer trophic interactions in Gulf of Mexico lower slope seep communities. PLoS One 8:e74459. doi:10.1371/journal.pone.0074459
  Article PubMed PubMed Central Google Scholar
• Bergquist D, Williams F, Fisher C (2000) Longevity record for deep-sea invertebrate. Nature 403:499–500
  Article CAS PubMed Google Scholar
• Bergquist D, Urcuyo I, Fisher C (2002) Establishment and persistence of seep vestimentiferan aggregations on the upper Louisiana slope of the Gulf of Mexico. Mar Ecol Prog Ser 241:89–98. doi:10.3354/meps241089
  Article Google Scholar
• Bergquist DC, Ward T, Cordes EE et al (2003) Community structure of vestimentiferan-generated habitat islands from Gulf of Mexico cold seeps. J Exp Mar Bio Ecol 289:197–222. doi:10.1016/S0022-0981(03)00046-7
  Article Google Scholar
• Bergquist D, Eckner J, Urcuyo I et al (2007) Using stable isotopes and quantitative community characteristics to determine a local hydrothermal vent food web. Mar Ecol Prog Ser 330:49–65. doi:10.3354/meps330049
  Article Google Scholar
• Cailliet G, Andrews A, Burton E et al (2001) Age determination and validation studies of marine fishes: do deep-dwellers live longer? Exp Gerontol 36:739–764. doi:10.1016/S0531-5565(00)00239-4
  Article CAS PubMed Google Scholar
• Childress JJ, Cowles DL, Favuzzi JA, Mickel TJ (1990) Metabolic rates of benthic deep-sea decapod crustaceans decline with increasing depth primarily due to the decline in temperature. Deep Sea Res Part A Oceanogr Res Pap 37:929–949. doi:10.1016/0198-0149(90)90104-4
  Article CAS Google Scholar
• Cordes EE, Bergquist DC, Shea K, Fisher CR (2003) Hydrogen sulphide demand of long-lived vestimentiferan tube worm aggregations modifies the chemical environment at deep-sea hydrocarbon seeps. Ecol Lett 6:212–219. doi:10.1046/j.1461-0248.2003.00415.x
  Article Google Scholar
• Cordes EE, Arthur MA, Shea K et al (2005) Modeling the mutualistic interactions between tubeworms and microbial consortia. PLoS Biol 3:e77. doi:10.1371/journal.pbio.0030077
  Article PubMed PubMed Central Google Scholar
• Cordes EE, Bergquist DC, Redding ML, Fisher CR (2007) Patterns of growth in cold-seep vestimenferans including Seepiophila jonesi: a second species of long-lived tubeworm. Mar Ecol 28:160–168. doi:10.1111/j.1439-0485.2006.00112.x
  Article Google Scholar
• Cordes EE, Bergquist DC, Fisher CR (2009) Macro-Ecology of Gulf of Mexico cold seeps. Annu Rev Mar Sci 1:143–168. doi:10.1146/annurev.marine.010908.163912
  Article Google Scholar
• Cordes EE, Becker EL, Fisher CR (2010) Temporal shift in nutrient input to cold-seep food webs revealed by stable-isotope signatures of associated communities. Limnol Oceanogr 55:2537–2548. doi:10.4319/lo.2010.55.6.2537
  Article Google Scholar
• Cowart DA, Halanych KM, Schaeffer SW, Fisher CR (2014) Depth-dependent gene flow in Gulf of Mexico cold seep Lamellibrachia tubeworms ( Annelida, Siboglinidae ). Hydrobiologia 736:139–154. doi:10.1007/s10750-014-1900-y
  Article CAS Google Scholar
• Dattagupta S, Miles LL, Barnabei MS, Fisher CR (2006) The hydrocarbon seep tubeworm Lamellibrachia luymesi primarily eliminates sulfate and hydrogen ions across its roots to conserve energy and ensure sulfide supply. J Exp Biol 209:3795–3805. doi:10.1242/jeb.02413
  Article CAS PubMed Google Scholar
• Deweerdt S (2012) Comparative biology: looking for a master switch. Nature 492:S10–S11. doi:10.1038/492S10a
  Article CAS PubMed Google Scholar
• Drazen JC, Seibel BA (2007) Depth-related trends in metabolism of benthic and benthopelagic deep-sea fishes. Limnol Oceanogr 52:2306–2316. doi:10.4319/lo.2007.52.5.2306
  Article CAS Google Scholar
• Fisher CR (1990) Chemoautotrophic and methanotrophic symbioses in marine invertebrates. Rev Aquat Sci 2:399–436
  CAS Google Scholar
• Ingram WC, Meyers SR, Brunner CA, Martens CS (2010) Late Pleistocene–Holocene sedimentation surrounding an active seafloor gas-hydrate and cold-seep fi eld on the Northern Gulf of Mexico Slope. Mar Geol 278:43–53. doi:10.1016/j.margeo.2010.09.002
  Article CAS Google Scholar
• Kirkwood TB, Austad SN (2000) Why do we age? Nature 408:233–238. doi:10.1038/35041682
  Article CAS PubMed Google Scholar
• Kohyama T, Takada T (1998) Recruitment rates in forest plots: Gf estimates using growth rates and size distributions. J Ecol 86:633–639
  Article Google Scholar
• McClain CR, Allen AP, Tittensor DP, Rex MA (2012) Energetics of life on the deep seafloor. Proc Natl Acad Sci 109:15366–15371. doi:10.1073/pnas.1208976109
  Article CAS PubMed PubMed Central Google Scholar
• McCoy MW, Gillooly JF (2008) Predicting natural mortality rates of plants and animals. Ecol Lett 11:710–716. doi:10.1111/j.1461-0248.2008.01190.x
  Article PubMed Google Scholar
• Paull CK, Jull AJT, Toolin LJ, Linick T (1985) Stable isotope evidence for chemosynthesis in an abyssal seep community. Nature 317:709–711. doi:10.1038/317709a0
  Article CAS Google Scholar
• Ravaux J, Zbinden M, Voss-Foucart MF et al (2003) Comparative degradation rates of chitinous exoskeletons from deep-sea environments. Mar Biol 143:405–412. doi:10.1007/s00227-003-1086-8
  Article CAS Google Scholar
• Ridgway ID, Richardson CA (2011) Arctica islandica: the longest lived non colonial animal known to science. Rev Fish Biol Fish 21:297–310. doi:10.1007/s11160-010-9171-9
  Article Google Scholar
• Roark EB, Guilderson TP, Dunbar RB et al (2009) Extreme longevity in proteinaceous deep-sea corals. Proc Natl Acad Sci U S A 106:5204–5208. doi:10.1073/pnas.0810875106
  Article CAS PubMed PubMed Central Google Scholar
• Roberts HH, Aharon P (1994) Hydrocarbon-derived carbonate buildups of the northern Gulf of Mexico continental slope: a review of submersible investigations. Geo-Marine Lett 14:135–148. doi:10.1007/BF01203725
  Article CAS Google Scholar
• Robison B, Seibel B, Drazen J (2014) Deep-sea octopus (Graneledone boreopacifica) conducts the longest-known egg-brooding period of any animal. PLoS One 9:e103437. doi:10.1371/journal.pone.0103437
  Article PubMed PubMed Central Google Scholar
• SAS Institute Inc, Cary NC (1989-2013) JMP®, Version 11
• Williams GC (1957) Pleiotropy, natural selection, and the evolution of senescence. Evolution (N Y) 11:398–411
  Google Scholar

Download references

Acknowledgements

This research was one part of a larger study led by Dr. Jim Brooks of TDI-Brooks that was jointly funded under the National Oceanographic Partnership Program (NOPP) by the US Bureau of Ocean Energy Management (BOEM), contract #0105CT39187, and the National Oceanic and Atmospheric Administration’s Office of Ocean Exploration and Research (NOAA OER). Many thanks to Erin Becker, Jeremy Potter, Liz Goehring, and Cindy Peterson for spending countless hours measuring tubeworms and to Stephanie Lessard-Pilon for her preliminary analysis of the tubeworm tag data. Collecting these tubeworms would not have been possible without the assistance of the captains and crew of the R/V Atlantis and NOAA Ship Ronald Brown and the crew and pilots of the DSV Alvin and ROV Jason II. We would also like to thank our anonymous reviewers for their valuable comments on improving this manuscript.

Author information

Authors and Affiliations

1. Temple University, Philadelphia, PA, USA
   Alanna Durkin & Erik E. Cordes
2. Pennsylvania State University, State College, PA, USA
   Charles R. Fisher

Authors

1. Alanna Durkin
   You can also search for this author inPubMed Google Scholar
2. Charles R. Fisher
   You can also search for this author inPubMed Google Scholar
3. Erik E. Cordes
   You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence toAlanna Durkin.

Additional information

Communicated by: Sven Thatje

Rights and permissions

About this article

Cite this article

Durkin, A., Fisher, C.R. & Cordes, E.E. Extreme longevity in a deep-sea vestimentiferan tubeworm and its implications for the evolution of life history strategies.Sci Nat 104, 63 (2017). https://doi.org/10.1007/s00114-017-1479-z

Download citation

• Received: 27 January 2017
• Revised: 09 June 2017
• Accepted: 11 June 2017
• Published: 08 July 2017
• DOI: https://doi.org/10.1007/s00114-017-1479-z

Keywords