Physiological responses to self-induced burrowing and metabolic rate depression in the ocean quahog Arctica islandica

Journal of Experimental Biology

Volumn 214, Issue 24, 2011, Pages 4223-4233

  Strahl, Julia ^a,b   Brey, Thomas ^a   Philipp, Eva E R ^c   Thorarinsdóttir, Gudrun ^d   Fischer, Natalie ^e   Wessels, Wiebke ^b   Abele, Doris ^a  

^a ALFRED WEGENER INSTITUTE FOR POLAR AND MARINE RESEARCH   (Germany)

^b UNIVERSITY OF BREMEN   (Germany)

^c UNIVERSITY OF KIEL   (Germany)

^d MARINE RESEARCH INSTITUTE   (Iceland)

^e HAMBURG UNIVERSITY OF APPLIED SCIENCES   (Germany)

Author keywords

Adenylates; Antioxidative enzymes; Arctica islandica; Burrowing; Mantle cavity water PO2; Metabolic rate depression; Reactive oxygen species formation; Succinate

Indexed keywords

ANTIOXIDANT; CATALASE; OXYGEN; REACTIVE OXYGEN METABOLITE; SUCCINIC ACID; SUPEROXIDE DISMUTASE;

ANIMAL; ANOXIA; ARTICLE; BASAL METABOLIC RATE; BIVALVE; ENZYMOLOGY; GILL; METABOLISM; OXIDATIVE STRESS; PHYSIOLOGY;

ANIMALS; ANOXIA; ANTIOXIDANTS; BASAL METABOLISM; BIVALVIA; CATALASE; GILLS; OXIDATIVE STRESS; OXYGEN; REACTIVE OXYGEN SPECIES; SUCCINIC ACID; SUPEROXIDE DISMUTASE;

EID: 83155181825     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.055178     Document Type: Article

References (59)

1. Abele, D., Strahl, J., Brey, T. and Philipp, E. E. R. (2008). Imperceptible senescence: ageing in the ocean quahog Arctica islandica. Free Radical Res. 42, 474-480. (Pubitemid 351935161)
2. Abele, D., Brey, T. and Philipp, E. (2009). Bivalve models of aging and the determination of molluscan lifespan. Exp. Gerontol. 44, 307-315.
3. Abele, D., Kruppe, M., Philipp, E. E. R. and Brey, T. (2010). Mantle cavity water oxygen partial pressure (PO2) in marine molluscs aligns with lifestyle. Can. J. Fish. Aquat. Sci. 67, 977-986.
4. Aebi, H. (1984). Catalase in vitro. Methods Enzymol. 105, 121-126.
5. Arntz, W. E. and Weber, W. (1970). Cyprina islandica L. (Molluska, Bivalvia) als Nahrung von Dorsch und Kliesche in der Kieler Bucht. Ber. Dtsch. Wiss. Komm. Meeresforsch. 21, 193-209.
6. Basova, L., Begum, S., Strahl, J., Sukhotin, A., Brey, T., Philipp, E. E. R. and Abele, D. (in press) Age-dependent patterns of antioxidants in Arctica islandica from six regionally separate populations with different life spans. Aquat. Biol. doi:10.3354/ab00387.
7. Begum, S., Basova, L., Strahl, J., Sukhotin, A., Heilmayer, O., Philipp, E., Brey, T. and 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.
8. Begum, S., Basova, L., Heilmayer, O. and Philipp, E. E. R. (2010). Growth and energy budget models of the bivalve Arctica islandica at six different sites in the Northeast Atlantic realm. J. Shellfish. Res. 29, 107-115.
9. Boutilier, R. G. and St-Pierre, J. (2000). Surviving hypoxia without really dying. Comp. Biochem. Physiol. A 126, 481-490.
10. Brey, T. (1991). Population dynamics of Sterechinus antarcticus (Echinodermata: Echinoidea) on the Weddell Sea shelf and slope, Antarctica. Antarc. Sci. 3, 251-256.
11. Brey, T., Pearse, J., Basch, L., MCCintock, J. and Slattery, M. (1995). Growth and production of Sterechinus neumayeri (Echinoidae: Echinodermata) in McMurdo Sound, Antarctica. Mar. Biol. 124, 279-292. (Pubitemid 26484170)
12. Brinkhoff, W., Stöckmann, K. and Grieshaber, M. (1983). Natural occurence of anaerobiosis in molluscs from intertidal habitats. Oecologia 1-2, 151-155. (Pubitemid 15274172)
13. Buttemer, W. A., Abele, D. and Constantini, D. (2010). From bivalves to birds: oxidative stress and longevity. Func. Ecol. 24, 971-983.
14. Cailliet, G. M., Andrews, A. H., Burton, E. J., Watters, D. L., Kline, D. E. and Ferry- Graham, L. A. (2001). Age determination and validation studies of marine fishes: do deep-dwellers live longer? Exp. Gerontol. 36, 739-764. (Pubitemid 32279582)
15. Diaz, J. R. and Rosenberg, R. (1995). Marine benthic hypoxia: a review of its ecological effects and the behavioural responses of benthic macrofauna. Oceanogr. Mar. Biol. Annu. Rev. 33, 245-303. (Pubitemid 26484137)
16. Epplé, V. M., Brey, T., Witbaard, R., Kuhnert, H. and Pätzold, J. (2006). Sclerochronological records of Arctica islandica from the inner German Bight. Holocene 16, 763-769. (Pubitemid 44196807)
17. Ghil, M., Allen, R. M., Dettinger, M. D., Ide, K., Kondrashov, D., Mann, M. E., Robertson, A., Saunders, A., Tian, Y., Varadi, F. et al. (2000). Advanced spectral methods for climatic time series. Rev. Geophys. 40, 3.1-3.41.
18. Griffith, C. L. and Richardson, C. A. (2006). Chemically induced predator avoidance behaviour in the burrowing bivalve Macoma balthica. J. Exp. Mar. Biol. Ecol. 331, 91-98.
19. Hermes-Lima, M. and Zenteno-Savín, T. (2002). Animal response to drastic changes in oxygen availability and physiological oxidative stress. Comp. Biochem. Physiol. C 133, 537-556. (Pubitemid 35373945)
20. Hermes-Lima, M., Storey, J. M. and Storey, K. B. (1998). Antioxidant defenses and metabolic drepression. The hypothesis of preparation for oxidative stress in land snails. Comp. Biochem. Physiol. B 129, 437-448. (Pubitemid 28386755)
21. Jónasson, J. P., Thórarinsdóttir, G. G., Eiríksson, H. and Marteinsdóttir, G. (2004). Temperature tolerance of Iceland scallop, Chlamys islandica (O. F. Muller) under controlled experimental conditions. Aquac. Res. 35, 1405-1414. (Pubitemid 39661328)
22. Kaasa, O. and Gudmundsson, K. (1994). Seasonal variation in the phytoplankton community in Eyafjördur, North Iceland. ICES C. M. L: 24, p. 15.
23. Kalivendi, S. V., Kotamraju, S., Cunningham, S., Shang, T. S., Hillard, C. J. and Kalyanaraman, B. (2003). 1-Methyl-4-phenylpyridinium (MPP+)-induced apoptosis and mitochondrial oxidant generation: role of transferrin-receptor- dependent iron and hydrogen peroxide. Biochem. J. 371, 151-164. (Pubitemid 36458089)
24. La Mesa, M. and Vacchi, M. (2001). Review. Age and growth of high Antarctic notothenioid fish. Antarc. Sci. 13, 227-235. (Pubitemid 32876113)
25. Larade, K. and Storey, K. B. (2009). Living without oxygen: anoxia-responsive gene expression and regulation. Curr. Genomics 10, 76-85.
26. Lazzarino, G., Amorini, A. M., Fazzina, G., Vagnozzi, R., Signoretti, S., Donzelli, S., Stasio, E. D., Giardina, B. and Tavazzi, B. (2003). Single-sample preparation for simultaneous cellular redox and energy state determination. Anal. Biochem. 322, 51-59. (Pubitemid 37188556)
27. Li, C. and Jackson, R. M. (2002). Reactive species mechanisms of cellular hypoxiareoxygenation injury. Am. J. Physiol. Cell Physiol. 282, 227-241.
28. Livingstone, D. R., De Zwaan, A., Leopold, M. and Marteijn, E. (1983). Studies on the phylogenetic distribution of pyruvate oxidoreductases. Biochem. Syst. Ecol. 11, 415-425.
29. Livingstone, D. R., Lips, F., Garcia Martinez, P. and Pipe, R. K. (1992). Antioxidant enzymes in the digestive gland of the common mussel Mytilus edulis. Mar. Biol. 112, 265-276.
30. Lushchak, V. I. and Bagnyukova, T. V. (2007). Hypoxia induces oxidative stress in issues of a goby, the rotan Perccottus glenii. Comp. Biochem. Physiol. Biochem. Mol. Biol. 148, 390-397. (Pubitemid 350026452)
31. Lushchak, V. I., Bagnyukova, T. V., Lushchak, O. V., Storey, J. M. and Storey, K. B. (2005). Hypoxia and recovery perturb free radical processes and antioxidant potential in common carp (Cyprinus carpio) tissues. Int. J. Biochem. Cell Biol. 37, 1319-1330. (Pubitemid 40381206)
32. Mann, M. E. and Lees, J. M. (1996). Robust estimation of background noise and signal detection in climatic time series. Clim. Change 33, 409-445.
33. Massabuau, J. C. (2003). Primitive, and protective, our cellular oxygenation status? Mech. Ageing Dev. 124, 857-863.
34. Michal, G., Beutler, H.-O., Lang, G. and Guentner, U. (1976). Enzymatic determination of succinic acid in foodstuffs. Z. Anal. Chem. 279, 137-138.
35. Morley, S. A., Lloyd, S. P., Miller, A. J. and Pörtner, H.-O. (2007). Hypoxia tolerance associated with activity reduction is a key adaptation for Laternula elliptica seasonal energetics. Ecophysiology 153, 29-36. (Pubitemid 47087373)
36. Oeschger, R. (1990). 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. 59, 133-143.
37. Oeschger, R. and Storey, K. B. (1993). Impact of anoxia and hydrogen sulphide on the metabolism of Arctica islandica L. (Bivalvia). J. Exp. Mar. Biol. Ecol. 170, 213-226. (Pubitemid 223035410)
38. Pauly, D. (2010). Gasping Fish And Panting Squids: Oxygen, Temperature And The Growth Of Water-Breathing Animals. Oldendorf/Luhe: International Ecology Institute.
39. Philipp, E., Pörtner, H.-O. and Abele, D. (2005). Mitochondrial ageing of a polar and a temperate mud clam. Mech. Ageing Dev. 126, 610-619. (Pubitemid 40461960)
40. Philipp, E., Heilmayer, O., Brey, T., Abele, D. and Pörtner, H.-O. (2006). Physiological ageing in a polar and a temperate swimming scallop. Mar. Ecol. Prog. Ser. 307, 187-198. (Pubitemid 43294009)
41. Ridgway, I. D. and Richardson, C. A. (2010). Arctica islandica: the longest lived non colonial animal known to science. Rev. Fish. Biol. Fish. 21, 297-310.
42. Rosenberg, R., Loo, L. O. and Möller, P. (1992). Hypoxia, salinity and temperature as structuring factors for marine benthic communities in a eutrophic area. Neth. J. Sea Res. 30, 121-129. (Pubitemid 24409352)
43. Schöne, B. R., Houk, S. D., Freyre Castro, A. D., Fiebig, J. and Oschman, W. (2005). Daily growth rates in shells of Arctica islandica: assessing sub-seasonal environmental controls on a long-lived Bivalve Mollusk. Palaios 20, 78-92. (Pubitemid 40263056)
44. Sidell, B. D., Driedzic, W. R., Stowe, D. B. and Johnston, I. A. (1987). Biochemical correlations of power development and metabolic fuel preference in fish hearts. Physiol. Zool. 60, 221-232.
45. Smith, W. H. F. and Sandwell, D. T. (1997). Global seafloor topography from satellite alimetry and ship septh soundings. Science 277, 1957-1962.
46. Sokal, R. R. and Rohlf, F. J. (1981). Biometry. The Principles and Practice of Statistics in Biological Research. San Francisco, CA: W. H. Freeman and Company.
47. Sokolova, I. M., Sokolov, E. P. and Ponnappa, K. M. (2005). Cadmium exposure affects mitochondrial bioenergetics and gene expression of key mitochondrial proteins in the eastern oyster Crassostrea virginica Gmelin (Bivalvia: Ostreidae). Aquat. Toxicol. 73, 242-255. (Pubitemid 40797579)
48. Strahl, J. and 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.
49. Strahl, J., Dringen, R., Schmidt, M. M., Hardenberg, S. and Abele, D. (2011). Metabolic and physiological responses in tissues of the long-lived bivalve Arctica islandica to oxygen deficiency. Comp. Biochem. Physiol. A 158, 513-519.
50. Taylor, A. C. (1976). Burrowing behaviour and anaerobiosis in the bivalve Arctica islandica (L.). J. Mar. Biol. Assoc. UK 56, 95-109.
51. Taylor, C. T. (2008). Mitochondria and cellular oxygen sensing in the HIF pathway. Biochem. J. 409, 19-25.
52. Tschischka, K., Abele, D. and Pörtner, H. O. (2000). Mitochondrial oxyconformity and cold adaptation in the polychaete Nereis Pelagica and the bivalve Arctica islandica from the Baltic and White Seas. J. Exp. Biol. 203, 3355-3368.
53. Vautard, R. and Ghil, M. (1989). Singular spectrum analysis in nonlinear dynamics, with applications to paleoclimatic time series. Physica D 35, 395-424.
54. Wanamaker, A. D., Heinemeier, J., Scourse, J. D., Richardson, C. A., Butler, P. G., Eiríksson, J. and Knudsen, K. L. (2008). Very long-lived molluscs confirm 17th century AD tephra-based radiocarbon reservoir ages for North Icelandic shelf waters. Radiocarbon 50, 399-412.
55. Wijsman, T. C. M. (1976). Adenosine phosphates and energy charge in different tissues of Mytilus edulis L. under aerobic and anaerobic conditions. J. Comp. Physiol. 107, 129-140.
56. Witbaard, R. and Klein, R. (1994). Long-term trends on the effects of the southern North Sea beam trawl fishery on the bivalve mollusc Arctica islandica L. (Mollusca, Bivalvia). ICES J. Mar. Sci. 51, 99-105. (Pubitemid 2075276)
57. Witbaard, R., Duineveld, G. C. A. and de Wilde, P. A. W. J. (1999). Geographical differences in growth rates of Arctica islandica (Molluska: Bivalvia) from the North Sea and adjacent waters. J. Mar. Biol. Assoc. U. K. 79, 907-915. (Pubitemid 29492439)
58. Zhao, H., Kalivendi, S., Zhang, H., Joseph, J. and Nithipatikom, K. (2003). Superoxide reacts with hydroethidine but forms a fluorescent product that is distinctly different from ethidium: potential implications in intracellular fluorescence detection of superoxide. Free Radic. Biol. Med. 34, 1359-1368. (Pubitemid 36570409)
59. Ziuganov, V., Miguel, E. S., Neves, R. J., Longa, A., Fernandez, C., Amaro, R., Beletsky, V., Popkovitch, E., Kaliuzhin, S. and Johnson, T. (2000). Life span variation of the freshwater pearl shell: a model species for testing longevity mechanisms in animals. Ambio 29, 102-105. (Pubitemid 30247316)