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High-latitude settings promote extreme longevity in fossil marine bivalves

  • David K. Moss (a1), Linda C. Ivany (a2), Robert B. Silver (a3), John Schue (a4) and Emily G. Artruc (a5)...
Abstract
Abstract

One of the longest-lived, noncolonial animals on the planet today is a bivalve that attains life spans in excess of 500 years and lives in a cold, seasonally food-limited setting. Separating the influence of temperature and food availability on life span in modern settings is difficult, as these two conditions covary. The life spans of fossil animals can provide insights into the role of environment in the evolution of extreme longevity that are not available from studies of modern taxa. We examine bivalves from the unique, nonanalogue, warm and high-latitude setting of Seymour Island, Antarctica, during the greenhouse intervals of the Late Cretaceous and Paleogene. Despite significant sampling limitations, we find that all 11 species examined are both slow growing and long-lived, especially when compared with modern bivalves living in similar temperature settings. While cool temperatures have long been thought to be a key factor in promoting longevity, our findings suggest an important role for caloric restriction brought about by the low and seasonal light regime of the high latitudes. Our life-history data, spanning three different families, emphasize that longevity is in part governed by environmental rather than solely phylogenetic or ecologic factors. Such findings have implications for both modern and ancient latitudinal diversity gradients, as a common correlate of slow growth and long life is delayed reproduction, which limits the potential for evolutionary change. While life spans of modern bivalves are well studied, data on life spans of fossil bivalves are sparse and largely anecdotal. Life histories of organisms from deep time can not only elucidate the controls on life span but also add a new dimension to our understanding of macroevolutionary patterns.

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D. Abele , J. Strahl , T. Brey , and E. Philipp . 2008. Imperceptible senescene: ageing in the ocean quahog Arctica islandica . Free Radical Research 42:474480.

D. Abele , T. Brey , and E. Philipp . 2009. Bivalve models of aging and the determination of molluscan lifespans. Experimental Gerontology 44:307315.

I. Ahn , J. Surh , Y. Park , H. Kwon , K. Choi , S. Kang , H. Choi , K. Kim , and H. Chung . 2003. Growth and seasonal energetics of the Antarctic bivalve Laternuala elliptica from King George Island, Antarctica. Marine Ecology Progress Series 257:99110.

J. Alroy 2010. Geographical, environmental and intrinsic biotic controls on Phanerozoic marine diversification. Palaeontology 53:12111235.

M. Alvarez , C. J. Del Rio , and S. Marenssi . 2014. Revision del genero Retrotapes del Rio (Bivalvia:Veneridae) en el Eoceno de la Antartida. Ameghiniana 51:6178.

M. J. Alvarez , and D. E. Pérez . 2016. Gerontic intraspecific variation in the Antarctic bivalve Retrotapes antarcticus . Ameghiniana 53:485494.

W. G. Ambrose , P. E. Renaud , W. L. Locke , F. R. Cottier , J. Berge , M. L. Carroll , B. Levin , and S. Ryan . 2011. Growth line deposition and variability in growth of two circumpolar bivalves (Serripes groenlandicus, and Clinocardium ciliatum). Polar Biology 35:345354.

R. B. Aronson , D. B. Blake , and T. Oji . 1997. Retrograde community structure in the late Eocene of Antarctica. Geology 25:903906.

R. B. Aronson , R. M. Moody , L. C. Ivany , D. B. Blake , J. E. Werner , and A. Glass . 2009. Climate change and trophic response of the Antarctic bottom fauna. PLoS ONE 4:e4385.

K. R. Arrigo , G. L. van Dijken , and S. Bushinsky . 2008. Primary production in the Southern Ocean, 1997–2006. Journal of Geophysical Research 113:127.

S. N Austad . 1989. Life extension by dietary restriction in the bowl and doil spider, Frontinella pyramitela . Experimental Gerontology 24:8392.

D. K. A. Barnes , and A. Clarke . 1995. Seasonality of feeding activity in Antarctic suspension feeders. Polar Biology 15:335340.

M. D. Bertness , S. D. Garrity , and S. C. Levings . 1981. Predation pressure and gastropod foraging: a tropical-temperate comparison. Evolution 35:9951007.

A. G. Beu 2009. Before the ice: biogeography of Antarctic Paleogene molluscan faunas. Palaeogeography, Palaeoclimatology, Palaeoecology 284:191226.

S. Brandhorst , I. Y. Choi , M. Wei , C. W. Cheng , S. Sedrakyan , G. Navarrete , L. Dubeau , L. P. Yap , R. Park , M. Vinciguerra , S. Di Biase , H. Mirzaei , M. G. Mirisola , P. Childress , L. Ji , S. Groshen , F. Penna , P. Odetti , L. Perin , P. S. Conti , Y. Ikeno , B. K. Kennedy , P. Cohen , T. E. Morgan , T. B. Dorff , and V. D. Longo . 2015. A periodic diet that mimics fasting promotes multi-system regeneration, enhanced cognitive performance, and healthspan. Cell Metabolism 22:8699.

T. Brey , and A. Clarke . 1993. Population dynamics of marine benthic invertebrates in Antarctic and subantarctic environments: are there unique adaptations? Antarctic Science 5:253266.

T. Brey , and A. Mackensen . 1997. Stable isotopes prove shell growth bands in the Antarctic bivalve Laternual elliptica to be formed annually. Polar Biology 17:465468.

T. Brey , L. S. Peck , J. Gutt , S. Hain , and W. E. Arntz . 1995. Population dynamics of Magellania fragilis, a brachiopod dominating a mixed-bottom macrobenthic assemblage on the Antarctic shelf. Journal of the Marine Biological Association of the United Kingdom 75:857869.

S Brockington . 2001. The seasonal energetics of the Antarctic bivalve Laternaula elliptica (King and Broderip) at Rother Point, Adelaide Island. Polar Biology 24:523530.

S. Brockington , and A. Clarke . 2001. The relative influence of temperature and food on the metabolism of a marine invertebrate. Journal of Experimental Marine Biology and Ecology 258:8799.

E. Brodte , R. Knust , H. O. Pörtner , and W. E. Arntz . 2006. Biology of the Antarctic eelpout Pachycara brachycephalum . Deep-Sea Research, part II (Topical Studies in Oceanography) 53:11311140.

D. P. Buick , and L. C. Ivany . 2004. 100 years in the dark: Extreme longevity of Eocene bivalves from Antarctica. Geology 32:921924.

P. G. Butler , A. D. Wanamaker , J. D. Scourse , C. A. Richardson , and D. J. Reynolds . 2013. Variability of marine climate on the North Icelandic Shelf in a 1357-year proxy archive based on growth increments in the bivalve Arctica islandica . Palaeogeography, Palaeoclimatology, Palaeoecology 373:141151.

L. Camus , B. Gulliksen , M. H. Depledge , and M. B. Jones . 2005. Polar bivalves are characterized by high antioxidant defences. Polar Research 24:111118.

G Clark . 1974. Growth lines in invertebrate skeletons. Annual Review of Earth and Planetary Science 2:7799.

R. J. Colman , T. M. Beasley , J. W. Kemnitz , S. C. Johnson , R. Weindruch , and R. M. Anderson . 2014. Caloric restriction reduces age-related and all-cause mortality in rhesus monkeys. Nature Communications 5:3557.

T. A. Dexter , and M. Kowalewski . 2013. Jackknife-corrected parametric bootstrap estimates of growth rates in bivalve mollusks using nearest living relatives. Theoretical Population Biology 90:3648.

E. Dudley , and G. Vermeij . 1980. Predation in time and space: drilling in the gastropod Turritella . Paleobiology 4:436441.

A. Dutton , B. T. Huber , K. C. Lohmann , and W. J. Zinsmeister . 2007. High-resolution stable isotope profiles of a dimitobelid belemnite: implications for paleodepth habitat and late Maastrichtian climate seasonality. Palaios 22:642650.

A. L. Dutton , K. C. Lohmann , and W. J. Zinsmeister . 2002. Stable isotope and minor element proxies for Eocene climate of Seymour Island, Antarctica. Paleoceanography 17(2), 113.

J. E. Francis , and I. Poole . 2002. Cretaceous and early Tertiary climates of Antarctica: evidence from fossil wood. Palaeogeography, Palaeoclimatology, Palaeoecology 182:4764.

A. L. Freestone , R. W. Osman , G. M. Ruiz , and M. E. Torchin . 2011. Stronger predation in the tropics shapes species richness patterns in marine communitites. Ecology 92:983993.

J. F. Gillooly , J. H. Brown , G. B. West , V. M. Savage , and E. L. Charnov . 2001. Effects of size and temperature on metabolic rate. Science 293:22482251.

D. H. Goodwin , K. W. Flessa , B. R. Schöne , and D. L. Dettman . 2001. Cross-calibration of daily growth increments, stable isotope variation, and temperature in the Gulf of California bivalve mollusk Chione cortezi: implications for paleoenvironmental analysis. Palaios 16:387398.

N. Hallmann , B. R. Schöne , A. Strom , and J. Fiebig . 2008. An intractable climate archive—sclerochronological and shell oxygen isotope analyses of the Pacific geoduck, Panopea abrupta (bivalve mollusk) from Protection Island (Washington State, USA). Palaeogeography, Palaeoclimatology, Palaeoecology 269:115126.

E. M. Harper , and L. Peck . 2016. Latitudinal and depth gradients in marine predation pressure. Global Ecology and Biogeography 25:670678.

W. W. Hay , and S. Floegel . 2012. New thoughts about the Cretaceous climate and oceans. Earth-Science Reviews 115:262272.

H Hillebrand . 2004. On the generality of the latititudinal diversity gradient. American Society of Naturalists 163:192211.

L. C. Ivany , and B. Runnegar . 2010. Early Permian seasonality from bivalve 18O and implications for the oxygen isotopic composition of seawater. Geology 38:10271030.

L. C. Ivany , K. C. Lohmann , F. Hasiuk , D. Blake , A. Glass , R. Aronson , and R. Moody . 2008. Eocene climate record of a high souther latitude continental shelf: Seymour Island, Antarctica. Geological Society of America Bulletin 120:659678.

D. S Jones . 1980. Annual cycle of shell growth increment formation in two continental shelf bivalves and its paleoecologic significance. Paleobiology 6:331340.

D. S. Jones , and S. J. Gould . 1999. Direct measurement of age in fossil Gryphaea: the solution to a classic problem in heterochrony. Paleobiology 25:158187.

D. S. Jones , and I. R. Quitmyer . 1996. Marking time with bivalve shells: oxygen isotopes and season of annual increment formation. Palaios 11:340346.

D. S. Jones , I. Thompson , and W. G. J. Ambrose . 1978. Age and growth rate determinations for the Atlantic surf clam Spisula solidissima (Bivalvia: Mactracea), based on interal growth lines in shell cross-sections. Marine Biology 47:6370.

D. S. Jones , D. F. Williams , and M. A. Arthur . 1983. Growth history and ecology of the Atlantic surf clam, Spisula solidissima (Dillwyn), as revealed by stable isotopes and shell increments. Journal Experimental Marine Biology and Ecology 73:225242.

D. S. Jones , M. A. Arthur , and D. J. Allard . 1989. Sclerochronological records of temperature and growth from shells of Mercenaria mercenaria from Narragansett Bay, Rhode Island. Marine Biology 102:225234.

D. B. Kemp , S. A. Robinson , J. A. Crame , J. E. Francis , J. Ineson , R. J. Whittle , V. Bowman , and C. O’Brien . 2014. A cool temperate climate on the Antarctic Peninsula through the latest Cretaceous to early Paleogene. Geology 42:583586.

M Klass . 1977. Aging in the nematode Caenorhabditis elegans: major biological and enivronmental factors influencing life span. Mechanisms of Ageing and Development 6:413429.

D. E. Krantz , D. S. Jones , and D. F. Williams . 1984. Growth rates of the sea scallop, Placopecten magellanicus, determine from the 18O/16O record in shell calcite. Biological Bulletin 167:186199.

B. Lakowski , and S. Hekimi . 1996. Determination of life-span in Caenorhabditis elegans by four clock genes. Science 272:10101013.

D. E. Lewis , and R. M. Cerrato . 1997. Growth uncoupling and the relationship between shell growth and metabolism in the soft shell clam Mya arenaria . Marine Ecology Progress Series 158:177189.

B. J. Lomovasky , T. Brey , E. Morriconi , and J. Calvo . 2002. Growth and reproduction of the venerid bivalve Eurhomalea exalbida in the Beagle Channel, Tierra del Fuego. Journal of Sea Research 48:209216.

R. A. Lutz , and M. C. Rhoads . 1980. Growth patterns within the molluscan shell: an overview. Pp. 203254. in M. C. Rhoads, and R. A. Lutz, eds. Skeletal growth of aquatic organisms: biological records of environmental change. Plenum, New York.

B. MacDonald , and M. Thomas . 1980. Age determination of the soft-shell clam Mya arenaria using shell internal growth lines. Marine Biology 58:105109.

C Macellari 1988. Stratigrpahy, sedimentology, and paleoecology of Upper Cretaceous/Paleocene shelf-deltaic sediments of Seymour Island. Geological Society of America Memoir 169:2533.

C. R Marshall . 1995. Distinguishing between sudden and gradual extinctions in the fossil record: predicting the position of the Cretaceous–Tertiary iridium anomaly using the ammonite fossil record on Seymour Island, Antarctica. Geology 23:731734.

E. J Masoro . 2000. Caloric restriction and aging: an update. Experimental Gerontology 35:299305.

M. J. Mette , A. D. Wanamaker , M. L. Carroll , W. G. Ambrose , and M. J. Retelle . 2016. Linking large-scale climate variability with Arctica islandica shell growth and geochemistry in northern Norway. Limnology and Oceanography 61:748764.

I. O. Norton , and J. G. Sclater . 1979. A model for the evolution of the Indian Ocean and the breakup of Gondwanaland. Journal of Geophysical Research (Solid Earth) 84:68036830.

G Pannella . 1976. Tidal growth patterns in recent and fossil mollusc bivalve shells: a tool for the reconstruction of paleotides. Naturwissenschaften 63:539543.

L. S. Peck , S. Brockington , and T. Brey . 1997. Growth and metabolism in the Antarctic brachiopod Liothyrella unva . Philosophical Transactions of the Royal Society of London B 352:851858.

L. S. Peck , P. Convey , and D. K. Barnes . 2006. Environmental constraints on life histories in Antarctic ecosystems: tempos, timings and predictability. Biological Reviews of the Cambridge Philosophical Society 81:75109.

G. B Picken . 1980. The distribution, growth, and reproduction of the Antarctic Limpet Nacella (Patinigera) concinna (Strebel, 1908). Journal of Experimental Marine Biology and Ecology 42:7185.

S Porebski 2000. Shelf-valley compound fill produced by fault subsidence and eustatic sea-level changes, Eocene La Meseta Formation, Seymour Island, Antarctica. Geology 28:147150.

D. C. Rhoads , and G. Pannnella . 1970. The use of molluscan shell growth patterns in ecology and paleoecology. Lethaia 3:143161.

C. A. Richardson , D. J. Crisp , N. W. Runham , and L. D. Gruffydd . 1980. The use of tidal growth bands in the shell of Cerastoderma edule to measure seasonal growth rates under cool temperate and sub-Arctic conditions. Journal of the Marine Biological Association of the United Kingdom 60:977989.

I. Ridgway , T. J. Bowden , A. Roman-Gonzalez , and C. A. Richardson . 2014. Resistance to oxidative stress is not associated with the exceptional longevity of the freshwater pearl mussel, Margaritifera margaritifera nor three unionid species. Aquatic Sciences 76:259267.

S Sato . 1994. Analysis of the relationship between growth and sexual maturation in Phacosoma japonicum (Bivalvia: Veneridae). Marine Biology 118:663672.

S Sato 1999. Temporal change of life-history traits in fossil bivalves: an example of Phacosoma japonicum from the Pleistocene of Japan. Palaeogeography, Palaeoclimatology, Palaeoecology 154:313323.

W. Sato-Okoshi , and K. Okoshi . 2007. Characteristics of shell microstructure and growth analysis of the Antarctic bivalve Laternula elliptica from Lützow-Holm Bay, Antarctica. Polar Biology 31:131138.

D. W. Schemske , G. G. Mittelbach , H. V. Cornell , J. M. Sobel , and K. Roy . 2009. Is there a latitudinal gradient in the importance of biotic interactions? Annual Review of Ecology, Evolution, and Systematics 40:245269.

B. R. Schöne , and D. P. Gillikin . 2013. Unraveling environmental histories from skeletal diaries—advances in sclerochronology. Palaeogeography, Palaeoclimatology, Palaeoecology 373:15.

B. R. Schöne , E. Dunca , J. Fiebig , and M. Pfeiffer . 2005a. Mutvei’s solution: an ideal agent for resolving microgrowth structures of biogenic carbonates. Palaeogeography, Palaeoclimatology, Palaeoecology 228:149166.

B. R. Schöne , S. D. Houk , A. D. Freyre Castro , J. Fiebig , W. Oschmann , I. Kroncke , W. Dreyer , and F. Gosselck . 2005b. Daily growth rates in shells of Arctica islandica: assessing sub-seasonal environmental controls on a long-lived bivalve mollusk. Palaios 20:7892.

B. R. Schöne , Z. Zhang , P. Radermacher , J. Thébault , D. E. Jacob , E. V. Nunn , and A.-F. Maurer . 2011. Sr/Ca and Mg/Ca ratios of ontogenetically old, long-lived bivalve shells (Arctica islandica) and their function as paleotemperature proxies. Palaeogeography, Palaeoclimatology, Palaeoecology 302:5264.

M. K. Sejr , M. K. Sand , K. T. Jensen , J. K. Peterson , P. B. Christensen , and S. Rysgaard . 2002b. Growth and production of Hiatella arctica (Bivalvia) in a high-Arctic fjord (Young Sound, Northeast Greenland). Marine Ecology Progress Series 244:163169.

W. Smith , J. Marra , M. Hiscock , and R. Barber . 2000. The seasonal cycle of phytoplankton bimoass and primary producitivty in the Ross Sea, Antarctica. Deep-Sea Research, part II (Topical Studies in Oceanography) 47:31193140.

J R. Speakman . 2005. Body size, energy metabolism and lifespan. Journal of Experimental Biology 208:17171730.

J. A. Thomas , J. J. Welch , R. Lanfear , and L. Bromham . 2010. A generation time effect on the rate of molecular evolution in invertebrates. Molecular Biology and Evolution 27:11731180.

T. S. Tobin , and P. D. Ward . 2015. Carbon isotope (δ13C) differences between Late Cretaceous ammonites and benthic mollusks from Antarctica. Palaeogeography, Palaeoclimatology, Palaeoecology 428:5057.

T. H. Torsvik , R. D. Müller , R. Van der Voo , B. Steinberger , and C. Gaina . 2008. Global plate motion frames: toward a unified model. Reviews of Geophysics 46(3).

W Van Voorhies . 2001. Metabolism and lifespan. Experimental Gerontology 36:5564.

C. Verdone-Smith , and H. E. Enesco . 1982. The effect of temperature and of dietary restriction on lifespan and reproduction in the rotifer Asplanchia brightwelli . Experimental Gerontology 17:252262.

C. C. Visaggi , and P. H. Kelley . 2015. Equatorward increase in naticid gastropod drilling predation on infaunal bivalves from Brazil with paleontological implications. Palaeogeography, Palaeoclimatology, Palaeoecology 438:285299.

I. Vladimirova , S. Kleimenova , and L. Radzinskaya . 2003. The relation of energy metabolism and body weight in bivalves (Mollusca:Bivalvia). Biology Bulletin 30:392399.

A. D. Wanamaker , J. Heinemeier , J. Scourse , C. Richardson , P. G. Butler , J. Eiriksson , and K. L. Knudsen . 2008. Very long-lived mollusks confirm 17th century AD tephra based radiocarbon reservoir ages for north Icelandic shelf waters. Radiocarbon 50:399412.

D. F. Williams , M. A. Arthur , D. S. Jones , and N. H. Williams . 1982. Seasonality and mean annual sea surface temperatures from isotopic and sclerochronological records. Nature 296:432434.

R. Witbaard , M. I. Jenness , K. van der Borg , and G. Ganssen . 1994. Verification of annual growth increments in Arctica islandica L. from the North Sea by means of oxygen and carbon isotopes. Netherlands Journal of Sea Research 33:91101.

J. D. Witts , V. C. Bowman , P. B. Wignall , J. Alistair Crame , J. E. Francis , and R. J. Newton . 2015. Evolution and extinction of Maastrichtian (Late Cretaceous) cephalopods from the López de Bertodano Formation, Seymour Island, Antarctica. Palaeogeography, Palaeoclimatology, Palaeoecology 418:193212.

J. D. Witts , R. J. Whittle , P. B. Wignall , J. A. Crame , J. E. Francis , R. J. Newton , and V. C. Bowman . 2016. Macrofossil evidence for a rapid and severe Cretaceous-Paleogene mass extinction in Antarctica. Nature Communications 7:11738.

A. D Woodhead . 1985. Feral fishes. Interdisciplinary Topics in Gerontology 21:2250.

J. Zachos , M. Pagani , L. Sloan , E. Thomas , and K. Billups . 2001. Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292:686692.

J. C. Zachos , G. R. Dickens , and R. E. Zeebe . 2008. An early Cenozoic perspective on greenhouse warming and carbon-cycle dynamics. Nature 451:279283.

W. J Zinsmeister . 1982. Review of the Upper Cretaceous–Lower Tertiary sequence on Seymour Island, Antarctica. Journal of the Geological Society 139:779785.

W. J. Zinsmeister , R. M. Feldmann , M. O. Woodburne , and D. H. Elliot . 1989. Latest Cretaceous/Earliest Tertiary transition on Seymour Island, Antarctica. Journal of Paleontology 63:731738.

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