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.
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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
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
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
Bergquist D, Williams F, Fisher C (2000) Longevity record for deep-sea invertebrate. Nature 403:499–500
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
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
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
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
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
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
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
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
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
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
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
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
Deweerdt S (2012) Comparative biology: looking for a master switch. Nature 492:S10–S11. doi:10.1038/492S10a
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
Fisher CR (1990) Chemoautotrophic and methanotrophic symbioses in marine invertebrates. Rev Aquat Sci 2:399–436
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
Kirkwood TB, Austad SN (2000) Why do we age? Nature 408:233–238. doi:10.1038/35041682
Kohyama T, Takada T (1998) Recruitment rates in forest plots: Gf estimates using growth rates and size distributions. J Ecol 86:633–639
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
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
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
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
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
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
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
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
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
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.
Communicated by: Sven Thatje
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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
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