Free Access
Gerontology 2010;56:55–65
(DOI:10.1159/000221004)

Masters of Longevity: Lessons from Long-Lived Bivalves – A Mini-Review

Philipp E.E.R.a · Abele D.b
aInstitute for Clinical Molecular Biology, Christian Albrecht University Kiel, Kiel, and bAlfred Wegener Institute for Polar and Marine Research, Bremerhaven, Germany
email Corresponding Author


 goto top of outline Key Words

  • Longevity
  • Ageing
  • Bivalves

 goto top of outline Abstract

The individual ages of bivalve molluscs can be inferred from the age rings laid down every year in the shell, especially in species inhabiting areas with seasonal variability in environmental factors such as food supply and temperature. Animals obtained from different environmental settings can therefore be used to investigate how specific environmental factors shape the process of ageing in this animal class. Some bivalves have extraordinary long life spans. Species like the ocean quahog Arctica islandica and the freshwater pearl mussel Margaritifera margaritifera live for over hundreds of years. Few studies so far have attempted to study the process of ageing, either specifically in long-lived bivalves or generally in very long-lived species. This review summarizes the current knowledge of cellular ageing in bivalves with a focus on the antioxidant system, as well as tissue repair and metabolic capacities of extremely long-lived species. We discuss the applicability of these animals as models for different ageing theories. We recommend a focus of future research on the molecular mechanisms potentially involved in supporting longevity in these species, including evolutionary old cellular mechanisms such as autophagy and apoptosis, as well as diverse cellular repair pathways.

Copyright © 2009 S. Karger AG, Basel


 goto top of outline References
  1. Hood L: Systems biology: integrating technology, biology, and computation. Mech Ageing Dev 2003;124:9–16.
  2. Kenyon C: The plasticity of aging: insights from long-lived mutants. Cell 2005;120:449–460.
  3. Zahn JM, Kim SK: Systems biology of aging in four species. Curr Opin Biotechnol 2007;18:355–359.
  4. Abele D: Toxic oxygen: the radical life-giver. Nature 2002;420:27.
  5. Theede H: Comparative studies on the influence of oxygen deficiency and hydrogen sulphide on marine bottom invertebrates. Neth J Sea Res 1973;7:244–252.
  6. Finch CE, Austad SN: History and prospects: symposium on organisms with slow aging. Exp Gerontol 2001;36:593–597.
  7. Ziuganov V, Miguel ES, Neves RJ, Longa A, Fernandez C, Amaro R, Beletsky V, Popkovitch E, Kaliuzhin S, Johnson T: Life span variation of the freshwater pearl shell: a model species for testing longevity mechanisms in animals. AMBIO 2000;29:102–105.

    External Resources

  8. Schöne BR, Fiebig J, Pfeiffer M, Gless R, Hickson J, Johnson ALA, Dreyer W, Oschmann W: Climate records from a bivalved Methuselah (Arctica islandica, mollusca; Iceland). Palaeogeogr Palaeoclimatol Palaeoecol 2005;228:130–148.

    External Resources

  9. Hedrick SM: The acquired immune system: a vantage from beneath. Immunity 2004;21:607–615.
  10. Richardson CA: Molluscs as archives of environmental change. Oceanogr Mar Biol 2001;39:103–164.

    External Resources

  11. Turekian KK, Cochran JK, Kharkar DP, Cerrato RM, Rimas Vaisnys J, Sanders HL, Grassle JF, Allen JA: Slow growth rate of a deep-sea clam determined by 228ra chronology. Proc Natl Acad Sci 1975;72:2829–2832.
  12. Anthony JL, Kesler DH, Downing WL, Downing JA: Length-specific growth rates in freshwater mussels (bivalvia: Unionidae): extreme longevity or generalized growth cessation? Freshw Biol 2001;46:1349–1359.
  13. Strom A, Francis RC, Mantua NJ, Miles EL, Peterson DL: North pacific climate recorded in growth rings of geoduck clams: a new tool for paleoenvironmental reconstruction. Geophys Res Lett 2004;31:L06206.

    External Resources

  14. Begum S, Basova L, Strahl J, Sukhotin A, Heilmayer O, Philipp EER, Brey T, Abele D: A metabolic model for the ocean quahog Arctica islandica – effects of animal mass and age, temperature, salinity and geography on respiration rate. J Shellfish Res, in press.
  15. Harman D: Aging: a theory based on free radical and radiation biology. J Gerontol 1956;11:298–300.
  16. Kruppe M, Philipp EER, Brey T, Abele D: Shell water oxygenation (PO2) in marine molluscs aligns with lifestyle: a ‘who is who’ in molluscan internal PO2. In review.
  17. Strahl J, Philipp E, Brey T, Broeg K, Abele D: Physiological aging in the ocean quahog Arctica islandica from Iceland. Aquat Biol 2007;1:77–83.

    External Resources

  18. Abele D, Strahl J, Brey T, Philipp EER: Imperceptible senescence: ageing in the ocean quahog Arctica islandica. Free Radical Res 2008;42:474–480.
  19. Sukhotin AA, Abele D, Poertner HO: Growth, metabolism and lipid peroxidation in Mytilus edulis: age and size effects. Mar Ecol Prog Ser 2002;226:223–234.
  20. Philipp E, Brey T, Poertner HO, Abele D: Chronological and physiological ageing in a polar and a temperate mud clam. Mech Ageing Dev 2005;126:589–609.
  21. Philipp EER, Schmidt M, Gsottbauer C, Saenger AM, Abele D: Size- and age-dependent changes in adductor muscle swimming physiology of the scallop Aequipecten opercularis. J Exp Biol 2008;211:2492–2501.
  22. Philipp E, Heilmayer O, Brey T, Abele D, Poertner HO: Physiological ageing in a polar and a temperate swimming scallop. Mar Ecol Prog Ser 2006;307:187–198.

    External Resources

  23. Ivanina AV, Sokolova IM, Sukhotin AA: Oxidative stress and expression of chaperones in aging mollusks. Comp Biochem Phys B 2008;150:53–61.
  24. Philipp E, Poertner HO, Abele D: Mitochondrial ageing of a polar and a temperate mud clam. Mech Ageing Dev 2005;126:610–619.
  25. Schmidt M, Philipp EER, Abele D: Size and age-dependent change of escape response from predator attack in the queen scallop Aequipecten opercularis. 2008;4:442–450.
  26. Longo VD: The Ras and Sch9 pathways regulate stress resistance and longevity. Exp Gerontol 2003;38:807–811.
  27. Thorarinsdottir G, Steingrimsson SA: Size and age at sexual maturity and sex ratio in ocean quahog, Arctica islandica (linnaeus, 1767), off northwest Iceland. J Shellfish Res 2000;19:943–947.
  28. Vina J, Borras C, Gambini J, Sastre J, Pallardo FV: Why females live longer than males: control of longevity by sex hormones. Sci Aging Knowl Environ 2005;23:17.
  29. Thompson I, Jones DS, Dreibelbis D: Annual internal growth banding and life history of the ocean quahog Arctica islandica (molluska: Bivalvia). Mar Biol 1980;57:25–43.

    External Resources

  30. Peterson CH: A concept of quantitative reproductive senility: application to the hard clam, Mercenaria mercenaria (l.)? Oecologia 1983;58:164–168.
  31. Vahl O: Age-specific residual reproductive value and reproductive effort in the iceland scallop, Chlamys islandica (O.F. Müller). Oecologia 1981;51:53–56.

    External Resources

  32. Breen P, Gabriel C, Tyson T: Preliminary estimates of age, mortality, growth, and reproduction in the hiatellid clam Panopea zelandica in New Zealand. NZ J Marine Freshw Res 1991;25:231–237.
  33. Bauer G: Reproductive strategy of the freshwater pearl mussel Margaritifera margaritifera. J Anim Ecol 1987;56:691–704.
  34. Terman A, Brunk UT: Oxidative stress, accumulation of biological ‘garbage’, and aging. Antioxid Redox Signal 2006;8:197–204.
  35. Yin D: Biochemical basis of lipofuscin, ceroid, and age pigment-like fluorophores. Free Radic Biol Med 1996;21:871–888.
  36. Oeschger R: Long-term anaerobiosis in sublittoral marine invertebrates from the western Baltic sea: Halicryptus spinulosus (Priapulida), Astarte borealis and Arctica islandica (Bivalvia). Mar Ecol Prog Ser 1990;59:133–143.
  37. Zwaan AD, Eertman RHM: Anoxic or aerial survival of bivalves and other euryoxic invertebrates as a useful response to environmental stress – a comprehensive review. Comp Biochem Physiology C 1996;113:299–312.
  38. Grune T, Jung T, Merker K, Davies KJA: Decreased proteolysis caused by protein aggregates, inclusion bodies, plaques, lipofuscin, ceroid, and ‘aggresomes’ during oxidative stress, aging, and disease. Int J Biochem Cell Biol 2004;36:2519–2530.
  39. Taylor AC: Burrowing behaviour and anaerobiosis in the bivalve Arctica islandica (l.). J Mar Biol Assoc UK 1976;56:95–109.

    External Resources

  40. Lomovasky BJ, Morriconi E, Brey T, Calvo J: Individual age and connective tissue lipofuscin in the hard clam Eurhomalea exalbida. J Exp Mar Biol Ecol 2002;276:83–94.
  41. Dunn K: Growth of endosymbiotic algae in the green hydra, Hydra viridissima. J Cell Sci 1987;88:571–578.

    External Resources

  42. Wiens M, Müller WEG: Cell death in porifera: molecular players in the game of apoptotic cell death in living fossils. Can J Zool 2006;84:307–321.
  43. Dunn SR, Schnitzler CE, Weis VM: Apoptosis and autophagy as mechanisms of dinoflagellate symbiont release during cnidarian bleaching: every which way you lose. Proc R Soc B Biol Sci 2007;274:3079–3085.
  44. Wagner C, Steffen R, Koziol C, Batel R, Lacorn M, Steinhart H, Simat T, Müller WEG: Apoptosis in marine sponges: a biomarker for environmental stress (cadmium and bacteria). Mar Biol 1998;131:411–421.
  45. Martinez DE: Mortality patterns suggest lack of senescence in hydra. Exp Gerontol 1998;33:217–225.
  46. Moore MN: Environmental distress signals: cellular reactions to marine pollution. Progr Histochem Cytochem 1991;23:2–19.
  47. Hole LM, Moore MN, Bellamy D: Age-related cellular and physiological reactions to hypoxia and hyperthermia in marine mussels. Mar Ecol Prog Ser 1995;122:173–178.
  48. Kefaloyianni E, Gourgou E, Ferle V, Kotsakis E, Gaitanaki C, Beis I: Acute thermal stress and various heavy metals induce tissue-specific pro- or anti-apoptotic events via the p38-mapk signal transduction pathway in Mytilus galloprovincialis (lam.). J Exp Biol 2005;208:4427–4436.
  49. Passos JF, Saretzki G, Zglinicki T: DNA damage in telomeres and mitochondri during cellular senescence: is there a connection? Nucleic Acids Res 2007;35:7505–7513.
  50. Machella N, Regoli F, Cambria A, Santella RM: Application of an immunoperoxidase staining method for detection of 7,8-dihydro-8-oxodeoxyguanosine as a biomarker of chemical-induced oxidative stress in marine organisms. Aquat Toxicol 2004;67:23–32.
  51. Frenzilli G, Nigro M, Scarcelli V, Gorbi S, Regoli F: DNA integrity and total oxyradical scavenging capacity in the Mediterranean mussel, Mytilus galloprovincialis: a field study in a highly eutrophicated coastal lagoon. Aquat Toxicol 2001;53:19–32.
  52. Accomando R, Viarengo A, Moore MN, Marchi B: Effects of ageing on nuclear DNA integrity and metabolism in mussel cells (Mytilus edulis l.). Int J Biochem Cell Biol 1999;31:443–450.
  53. Dixon DR, Wilson JT, Dixon LRJ: Toxic vents and DNA damage. Int Ridge Crest Res 2000;9:13–14.
  54. Pruski AM, Dixon DR: Toxic vents and DNA damage: first evidence from a naturally contaminated deep-sea environment. Aquat Toxicol 2003;64:1–13.
  55. Klapper W, Heidorn K, Kuhne K, Parwaresch R, Krupp G: Telomerase activity in ‘immortal’ fish. FEBS Lett 1998;434:409–412.
  56. Klapper W, Kuehne K, Singh KK, Heidorn K, Parwaresch R, Krupp G: Longevity of lobsters is linked to ubiquitous telomerase expression. FEBS Lett 1998;439:143–146.
  57. Forsyth NR, Wright WE, Shay JW: Telomerase and differentiation in multicellular organisms: turn it off, turn it on, and turn it off again. Differentiation 2002;69:188–197.
  58. Owen R, Sarkis S, Bodnar A: Developmental pattern of telomerase expression in the sand scallop, Euvola ziczac. Invertebr Biol 2007;126:40–45.

    External Resources

  59. Estabrooks SL: The possible role of telomeres in the short life span of the bay scallop, Argopecten irradians irradians (Lamarck 1819). J Shellfish Res 2007;26:307–313.

    External Resources

  60. Abele D, Philipp E, Gonzalez P, Puntarulo S: Marine invertebrate mitochondria and oxidative stress. Front Biosci 2007;12:933–946.
  61. Barber BJ: Neoplastic diseases of commercially important marine bivalves. Aquat Living Resour 2004;17:449–466.

    External Resources

  62. Elston RA, Kent ML, Drum AS: Transmission of hemic neoplasia in the bay mussel, Mytilus edulis, using whole cells and cell homogenate. Dev Compar Immunol 1988;12:719–727.
  63. Kent ML, Wilkinson MT, Drum AS, Elston RA: Failure of transmission of hemic neoplasia of bay mussels, Mytilus trossulus, to other bivalve species. J Invertebr Pathol 1991;57:435–436.
  64. Collins CM, Mulcahy MF: Cell-free transmission of a haemic neoplasm in the cockle Cerastoderma edule. Dis Aquatic Organ 2003;54:61–67.
  65. Barber BJ, MacCallum GS, Robinson SMC, McGladdery S: Occurrence and lack of transmissibility of gonadal neoplasia in softshell clams, Mya arenaria, in Maine (USA) and Atlantic Canada. Aquat Living Resour 2002;15:319–326.
  66. Abele D, Brey T, Philipp EER: Bivalve models of aging and the determination of molluscan lifespans. J Exp Gerontol, in press.
  67. Clegg J: Embryos of Artemia franciscana survive four years of continuous anoxia: the case for complete metabolic rate depression. J Exp Biol 1997;200:467–475.
  68. Hairston NG, Van Brunt RA, Kearns CM, Engstrom DR: Age and survivorship of diapausing eggs in a sediment egg bank. Ecology 1995;76:1706–1711.
  69. Geiser F: Metabolic rate and body temperature reduction during hibernation and daily torpor. Ann Rev Physiol 2004;66:239–274.
  70. Masoro EJ: Caloric restriction and aging: an update. Exp Gerontol 2000;35:299–305.
  71. Hermes-Lima M, Storey JM, Storey KB: Antioxidant defenses and metabolic depression: the hypothesis of preparation for oxidative stress in land snails. Comp Biochem Phys 1998;120:437–448.
  72. Ziuganov V: Mussel larvae-infected Atlantic salmon with canceled ‘death program’ and long lived arctic stickleback are potential sources of stress protectors and anticancer medication. Integrated Sci J 2006;13:56–68.
  73. Bauer G: Variation in the life span and size of the freshwater pearl mussel. J Anim Ecol 1992;61:425–436.
  74. Porter RK, Hulbert AJ, Brand MD: Allometry of mitochondrial proton leak: influence of membrane surface area and fatty acid composition. Am J Physiol 1996;271:R1550–R1560.
  75. Cossins AR, Christiansen J, Prosser CL: Adaptation of biological membranes to temperature. The lack of homeoviscous adaptation in the sarcoplasmic reticulum. Biochim Biophys Acta 1978;511:442–454.
  76. Peck L, Powell D, Tyler P: Very slow development in two Antarctic bivalve molluscs, the infaunal clam Laternula elliptica and the scallop Adamussium colbecki. Mar Biol 2007;150:1191–1197.

    External Resources

  77. Kirkwood TB, Austad SN: Why do we age? Nature 2000;408:233–238.
  78. Taylor AC: The cardiac responses to shell opening and closure in the bivalve Arctica islandica. J Exp Biol 1976;64:751–759.
  79. Hedgecock D, Gaffney PM, Goulletquer P, Guo X, Reece K, Warr GW: The case for sequencing the pacific oyster genome. J Shellfish Res 2005;24:429–441.

    External Resources

  80. Sauvage C, Bierne N, Lapègue S, Boudry P: Single nucleotide polymorphisms and their relationship to codon usage bias in the pacific oyster Crassostrea gigas. Gene 2007;406:13–11.
  81. Haussmann MF, Winkler DW, O’Reilly KM, Huntington CE, Nisbet ICT, Vleck CM: Telomeres shorten more slowly in long-lived birds and mammals than in short-lived ones. Proc Biol Sci 2003;270:1387–1392.
  82. Beaver PC: Light, long-lasting Necator infection in a volunteer. Am J Trop Med Hyg 1988;39:369–372.
  83. Kirkwood TB: Evolution of ageing. Nature 1977;270:301–304.
  84. Hayflick L: The limited in vitro lifetime of human diploid cell strains. Exp Cell Res 1965;37:614–636.

 goto top of outline Author Contacts

Eva E.R. Philipp, PhD
Institute for Clinical Molecular Biology, Christian Albrecht University Kiel
Schittenhelmstrasse 12
DE–24105 Kiel (Germany)
Tel. +49 431 597 1080, Fax +49 431 597 1842, E-Mail e.philipp@ikmb.uni-kiel.de


 goto top of outline Article Information

Received: December 23, 2008
Accepted: April 8, 2009
Published online: May 26, 2009
Number of Print Pages : 11
Number of Figures : 1, Number of Tables : 0, Number of References : 84


 goto top of outline Publication Details

Gerontology (International Journal of Experimental, Clinical, Behavioural and Technological Gerontology)

Vol. 56, No. 1, Year 2010 (Cover Date: January 2010)

Journal Editor: Wick G. (Innsbruck)
ISSN: 0304-324X (Print), eISSN: 1423-0003 (Online)

For additional information: http://www.karger.com/GER


Copyright / Drug Dosage / Disclaimer

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher or, in the case of photocopying, direct payment of a specified fee to the Copyright Clearance Center.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in goverment regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.