Lipofuscin accumulation in tissues of Arctica islandica indicates faster ageing in populations from brackish environments
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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.
KeywordsGerman Bight Standard Metabolic Rate Mantle Tissue Lipofuscin Granule Norwegian Coast
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.
Compliance with ethical standards
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 (22.214.171.1244, 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.
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
- Abele D, Brey T, Philipp EER (2016) Ecophysiology of extant marine Bivalvia. In: Carter J (ed) Treatise Online XX, pp 1–47Google Scholar
- 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 183–188Google Scholar
- Dudycha JL, Tessier AJ (1999) Natural genetic variation of life span, reproduction, and juvenile growth in Daphnia. Evolution:1744–1756Google Scholar
- 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:872–880Google Scholar
- Gosling E (2013) Bivalve molluscs: biology, ecology, and culture. Fishing news books. Blackwell, OxfordGoogle Scholar
- 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 420–431CrossRefGoogle Scholar
- Medawar PB (1952) An unsolved problem of biology. CollegeGoogle Scholar
- 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 163–186Google Scholar
- 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 126:589–609Google Scholar
- Saleuddin A (1964) Observations on the habit and functional anatomy of Cyprina islandica (L.). J Mollusc Stud 36:149–162Google Scholar
- Savinov V, Savinova T, Dahle S (2001) Contaminants. In: Berger V, Dahle S (eds) White sea. ecology and environment. Derzavets Publisher, S. Petersburg, pp 123–137Google Scholar
- 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 212:215–232CrossRefGoogle Scholar
- Sokal R, Rohlf F (1981) Biometry, WH Freeman, New YorkGoogle Scholar
- 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 CrossRefGoogle Scholar