Abstract
Environmental factors can affect the rate of ageing and shape the lifespan in marine ectotherms. The mechanisms and the degree of environmental influence on aging can best be studied in species with wide ranging biogeographic distribution. One of the biomarkers of physiological ageing is the fluorescent age pigment lipofuscin, which accumulates over lifetime in tissues of bivalves. We compared lipofuscin accumulation rate in muscles and respiratory tissues of the extremely long-lived bivalve Arctica islandica from five geographically distinct populations (Northern Norway, White Sea, Kiel Bay, German Bight and Iceland). Maximum investigated chronological age across different populations in the present study differed from 40 years in Kiel Bay to 192 years at Iceland. An inverse association between lipofuscin deposition rate and recorded maximum age was observed through inter-population comparisons. In most cases lipofuscin accumulated exponentially over age in a tissue-specific manner. The age-specific lipofuscin content was significantly higher in respiratory than muscles tissues in all populations. Cellular lipofuscin granule area can be used as indicator of aging across A. islandica populations with the variance in granule accumulation depending on the annual variations of salinity in different marine regions, but not on the habitat-specific thermal envelope.
Similar content being viewed by others
References
Aarab N, Pampanin D, Naevdal A, Øysæd K, Gastaldi L, Bechmann R (2008) Histopathology alterations and histochemistry measurements in mussel, Mytilus edulis collected offshore from an aluminium smelter industry (Norway). Mar Pollut Bull 57:569–574
Abele D, Puntarulo S (2004) Formation of reactive species and induction of antioxidant defence systems in polar and temperate marine invertebrates and fish. Comp Biochem Physiol Part A Mol Integr Physiol 138:405–415
Abele D, Brey T, Philipp EER (2009) Bivalve models of aging and the determination of molluscan lifespans. Exp Gerontol 44:307–315
Abele D, Brey T, Philipp EER (2016) Ecophysiology of extant marine Bivalvia. In: Carter J (ed) Treatise Online XX, pp 1–47
Austad SN (1993) Retarded senescence in an insular population of Virginia opossums (Didelphis virginiana). J Zool 229:695–708
Basova L, Begum S, Strahl J, Sukhotin A, Brey T, Philipp E, Abele D (2012) Age dependent patterns of antioxidants in Arctica islandica from six regionally separate populations with different life spans. Aquat Biol 14:141–152
Begum S, Basova L, Strahl J, Sukhotin A, Heilmayer O, Philipp E, Abele D (2009) 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 28:533–539
Bluhm BA, Brey T, Klages M (2001) The autofluorescent age pigment lipofuscin: key to age, growth and productivity of the Antarctic amphipod Waldeckia obesa (Chevreux, 1905). J Exp Mar Biol Ecol 258:215–235
Brenner M, Buchholz C, Heemken O, Buck BH, Köhler A (2012) Health and growth performance of the blue mussel (Mytilus edulis L.) from two hanging cultivation sites in the German Bight: a nearshore—offshore comparison. Aquacult Int 20:751–778
Brenner M, Broeg K, Frickenhaus S, Buck BH, Koehler A (2014) Multi-biomarker approach using the blue mussel (Mytilus edulis L.) to assess the quality of marine environments: season and habitat-related impacts. Mar Environ Res 95:13–27
Brunk UT, Terman A (2002) Lipofuscin: mechanisms of age-related accumulation and influence on cell function. Free Radic Biol Med 33:611–619
Butler PG, Wanamaker AD, Scourse JD, Richardson CA, Reynolds DJ (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. Palaeogeogr Palaeoclimatol Palaeoecol 373:141–151
Buttemer WA, Abele D, Costantini D (2010) From bivalves to birds: oxidative stress and longevity. Funct Ecol 24:971–983
Claussen U, Zevenboom W, Brockmann U, Topcu D, Bot P (2009) Assessment of the eutrophication status of transitional, coastal and marine waters within OSPAR. Hydrobiologia 629:49–58
Dahlgren T, Weinberg J, Halanych K (2000) Phylogeography of the ocean quahog (Arctica islandica): influences of paleoclimate on genetic diversity and species range. Mar Biol 137:487–495
Demina L, Martynova D, Podlesnyh K (2009) Accumulation of heavy metals in Kandalaksha Bay of the White Sea by various components of the ecosystem. In: Biological resources of the White Sea and inner waters of European North. KarNC RAN, Petrozavodsk, pp 183–188
Dudycha JL, Tessier AJ (1999) Natural genetic variation of life span, reproduction, and juvenile growth in Daphnia. Evolution:1744–1756
Finch C, Austad SN (2001) History and prospects: symposium on organisms with slow aging. Exp Gerontol 36:593–597
Fiori S, Defeo O (2006) Biogeographic patterns in life-history traits of the yellow clam, Mesodesma mactroides, in sandy beaches of South America. J Coast Res:872–880
Fleming J, Leon H, Miquel J (1981) Effects of ethidium bromide on development and aging of Drosophila: implications for the free radical theory of aging. Exp Gerontol 16:287–293
Glöckner G, Heinze I, Platzer M, Held C, Abele D (2013) The mitochondrial genome of Arctica islandica; phylogeny and variation. PLoS One 8:e82857
Gosling E (2013) Bivalve molluscs: biology, ecology, and culture. Fishing news books. Blackwell, Oxford
Gruber H et al (2015) Age-related cellular changes in the long-lived bivalve A. islandica. Age 37:1–12. doi:10.1007/s11357-015-9831-8
Guerra C, Zenteno-Savín T, Maeda-Martínez A, Abele D, Philipp E (2013) The effect of predator exposure and reproduction on oxidative stress parameters in the Catarina scallop Argopecten ventricosus. Comp Biochem Physiol Part A Mol Integr Physiol 165:89–96
Hansson D, Gustafsson E (2011) Salinity and hypoxia in the Baltic Sea since A.D. 1500. J Geophys Res Oceans 116. doi:10.1029/2010JC006676
Harman D (1956) Aging: a theory based on free radical and radiation biology. J Gerontol 11:298–300
Hiebenthal C, Philipp EE, Eisenhauer A, Wahl M (2013) Effects of seawater pCO2 and temperature on shell growth, shell stability, condition and cellular stress of Western Baltic Sea Mytilus edulis (L.) and Arctica islandica (L.). Mar Biol 160:2073–2087
Kagley AN, Snider R, Krishnakumar P, Casillas E (2003) Assessment of seasonal variability of cytochemical responses to contaminant exposure in the blue mussel Mytilus edulis (complex). Arch Environ Contam Toxicol 44:0043–0052. doi:10.1007/s00244-002-1303-3
Krishnakumar P, Casillas E, Varanasi U (1997) Cytochemical responses in the digestive tissue of Mytilus edulis complex exposed to microencapsulated PAHs or PCBs. Comp Biochem Physiol Part CPharmacol Toxicol Endocrinol 118:11–18
Lee S-J, Kenyon C (2009) Regulation of the longevity response to temperature by thermosensory neurons in Caenorhabditis elegans. Curr Biol 19:715–722
Liu RK, Walford RL (1970) Observations on the lifespans of several species of annual fishes and of the world’s smallest fishes. Exp Gerontol 5:241–246
Lushchak VI, Semchyshyn HM, Lushchak OV (2011) The classic methods to measure oxidative damage: lipid peroxides, thiobarbituric-acid reactive substances, and protein carbonyls. In: Abele D, Vázquez-Medina JP, Zenteno-Savín T (eds) Oxidative stress in aquatic ecosystems. Wiley-Blackwell, Chichester, pp 420–431
Medawar PB (1952) An unsolved problem of biology. College
Millward G, Rowley C, Sands T, Howland R, Pantiulin A (1999) Metals in the sediments and mussels of the Chupa Estuary (White Sea) Russia. Estuar Coast Shelf Sci 48:13–25
Munro D, Blier PU (2012) The extreme longevity of Arctica islandica is associated with increased peroxidation resistance in mitochondrial membranes. Aging cell 11:845–855
Mutvei H, Westermark T, Dunca E, Carell B, Forberg S, Bignert A (1994) Methods for the study of environmental changes using the structural and chemical information in molluscan shells. Bull de l’Institut Océanogr 163–186
Pearse AE (1961) Histochemistry: theoretical and applied. Am J Med Sci 241:136
Philipp EER, Abele D (2010) Masters of longevity? Lessons from long lived bivalves - review. Gerontology 56:55–65
Philipp E, Brey T, Pörtner H-O, Abele D (2005a) Chronological and physiological ageing in a polar and a temperate mud clam. Mech Ageing Dev 126:589–609
Philipp E, Pörtner H-O, Abele D (2005b) Mitochondrial ageing of a polar and a temperate mud clam. Mech Ageing Dev 126:610–619
Reznick DN, Bryant MJ, Roff D, Ghalambor CK, Ghalambor DE (2004) Effect of extrinsic mortality on the evolution of senescence in guppies. Nature 431:1095–1099
Ridgway I, Richardson C (2011) Arctica islandica: the longest lived non colonial animal known to science. Rev Fish Biol Fish 21:297–310
Saleuddin A (1964) Observations on the habit and functional anatomy of Cyprina islandica (L.). J Mollusc Stud 36:149–162
Savinov V, Savinova T, Dahle S (2001) Contaminants. In: Berger V, Dahle S (eds) White sea. ecology and environment. Derzavets Publisher, S. Petersburg, pp 123–137
Schöne BR, Castro ADF, Fiebig J, Houk SD, Oschmann W, Kröncke I (2004) Sea surface water temperatures over the period 1884–1983 reconstructed from oxygen isotope ratios of a bivalve mollusk shell (Arctica islandica, southern North Sea). Palaeogeogr Palaeoclimatol Palaeoecol 212:215–232
Sokal R, Rohlf F (1981) Biometry, WH Freeman, New York
Strahl J, Abele D (2010) Cell turnover in tissues of the long-lived ocean quahog Arctica islandica and the short-lived scallop Aequipecten opercularis. Mar Biol 157:1283–1292
Strahl J, Philipp E, Brey T, Broeg K, Abele D (2007) Physiological aging in the Icelandic population of the ocean quahog Arctica islandica. Aquat Biol 1:77–83
Swaileh K (1996) Seasonal variations in the concentrations of Cu, Cd, Pb and Zn in Arctica islandica L.(Mollusca: Bivalvia) from Kiel Bay, Western Baltic Sea. Mar Pollut Bull 32:631–635
Ungvari Z, Ridgway I, Philipp EE, Campbell CM, McQuary P, Chow T, Coelho M, Didier ES, Gelino S, Holmbeck MA, Kim I (2011) Extreme longevity is associated with increased resistance to oxidative stress in Arctica islandica, the longest-living non-colonial animal. Anim J Gerontol Biol Sci Med Sci 66A:741–750. doi:10.1093/gerona/glr044
Williams PD, Day T (2003) Antagonistic pleiotropy, mortality source interactions, and the evolutionary theory of senescence. Evol Int J org Evol 57:1478–1488
Ziuganov V, Miguel ES, Neves RJ, Longa A, Fernández C, Amaro R, Beletsky V, Popkovitch E, Kaliuzhin S, Johnson T (2000) Life span variation of the freshwater pearl shell: a model species for testing longevity mechanisms in animals. AMBIO A J Hum Environ 29:102–105
Acknowledgements
The authors thank the staff of histological laboratory of Angela Koehler (AWI, Bremerhaven, Germany) who kindly provided support for lipofuscin measurements. Thanks to Katja Broeg and Sieglinde Bahns for their help with the lipofuscin analysis. We are also grateful to the anonymous reviewers for their positive input which allowed us to improve the manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Funding
This work was supported by grants from the German Academic Exchange Service (A/05/56588, A/07/72522 to L.B.); Federal Ministry of Education and Research International Office (RUS-07/A11 to L.B.); Saint-Petersburg State University (1.38.253.2014, 1.42.1493.2015 and 1.42.1099.2016 to L.B.) and Russian Foundation for Basic Research (14-04-00466 to L.B. and A.S.).
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
Additional information
Responsible Editor: J. H. Stillman.
Reviewed by Undisclosed experts.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Basova, L., Strahl, J., Philipp, E.E.R. et al. Lipofuscin accumulation in tissues of Arctica islandica indicates faster ageing in populations from brackish environments. Mar Biol 164, 72 (2017). https://doi.org/10.1007/s00227-017-3110-4
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-017-3110-4