Hostname: page-component-669899f699-tpknm Total loading time: 0 Render date: 2025-04-25T00:37:11.271Z Has data issue: false hasContentIssue false
  • English
  • Français

Effects of sulphide on anoxia-driven mortality and anaerobic metabolism in the ark shell Anadara kagoshimensis

Published online by Cambridge University Press:  21 March 2016

Yasushi Miyamoto Open the ORCID record for Yasushi Miyamoto [Opens in a new window]  and
Chitose Iwanaga
Yasushi Miyamoto*
Affiliation:
Environmental Sanitation Research Center, Tottori Prefecture, 526-1, Minamidani, Yurihama-cho, Tottori 682-0704, Japan
Chitose Iwanaga
Affiliation:
Environmental Sanitation Research Center, Tottori Prefecture, 526-1, Minamidani, Yurihama-cho, Tottori 682-0704, Japan
*
Correspondence should be addressed to: Y. Miyamoto, Environmental Sanitation Research Center, Tottori Prefecture, 526-1, Minamidani, Yurihama-cho, Tottori, 682-0704, Japan Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Reduction in survival under hypoxic conditions in the presence of sulphide has been repeatedly demonstrated in various benthic invertebrates. However, the reason for this reduction has not yet been clearly elucidated. In this study, the effects of sulphide accumulation on anoxic survival and anaerobic metabolism were investigated in the ark shell Anadara kagoshimensis. Ark shells from western Japan were experimentally exposed to 3 sulphide-accumulation levels under sustained anoxic conditions: accumulated H2S treatment (static incubation), decreased H2S treatment (semi-static incubation with daily replacement of incubation media), and inhibited H2S treatment (static incubation with the addition of antibiotics). Moreover, the effect of antibiotics on anoxic survival was examined under sulphide exposure. The decreased H2S and inhibited H2S treatments resulted in 1.5- and 3-fold increase in the anoxic survival time, respectively, when compared with the accumulated H2S treatment. Under anoxic sulphide exposure, the antibiotics addition did not affect survival time, suggesting the shorter survival time in the accumulated H2S incubation was probably due to sulphide toxicity. Glycogen consumption and propionate accumulation, which indicate activation of anaerobic metabolism, were observed in both accumulated and inhibited H2S treatments. However, glycogen consumption was significantly higher in the accumulated H2S treatment after a significant sulphide accumulation was detected in the incubation media. In addition, survival in the accumulated H2S treatment decreased rapidly, whereas no significant mortality was observed in the inhibited H2S throughout the experiment. These results likely suggest that the accelerated anoxic-driven mortality in sulphide-rich environments was partly due to the faster breakdown of glycogen.

Keywords

Anadara kagoshimensisanaerobic metabolismglycogenhypoxiamortalitysulphide
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 97 , Issue 2 , March 2017 , pp. 329 - 336
Copyright
Copyright © Marine Biological Association of the United Kingdom 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

REFERENCES

Arndt, C. and Schiedek, D. (1997) Nephtys hombergii, a free living predator in marine sediments: energy production under environmental stress. Marine Biology 129, 643–650.Google Scholar
Arp, A.J., Childress, J.J. and Vetter, R.D. (1987) The sulfide-binding protein in the blood of the vestimentiferan tube-worm, Riftia pachyptila, is the extracellular haemoglobin. Journal of Experimental Biology 128, 139–158.Google Scholar
Babarro, J.M.F. and De Zwaan, A. (2008) Anaerobic survival potential of four bivalves from different habitats. A comparative survey. Comparative Biochemistry and Physiology, Part A 151, 108–113.Google Scholar
Carroll, N.V., Longley, R.W. and Roe, J.J. (1955) The determination of glycogen in liver and muscle by use of anthrone reagent. Journal of Biological Chemistry 220, 583–593.Google Scholar
Cline, J.D. (1969) Spectrophotometric determination of hydrogen sulfide in natural waters. Limnology and Oceanography 3, 454–458.Google Scholar
Conley, D.J., Carstensen, J., Vaquer-Sunyer, R. and Duarte, C.M. (2009) Ecosystems thresholds with hypoxia. Hydrobiologia 629, 21–29.CrossRefGoogle Scholar
De Zwaan, A., Babarro, J.M.F., Monari, M. and Cattani, O. (2002) Anoxic survival potential of bivalves: (arte)facts. Comparative Biochemistry and Physiology, Part A 131, 615–624.Google Scholar
De Zwaan, A., Cattan, O. and Puzer, V.M. (1993) Sulfide and cyanide-induced mortality and anaerobic metabolism in the arcid blood clam Scapharca inaequivalvis . Comparative Biochemistry and Physiology, Part C 105, 49–54.Google Scholar
De Zwaan, A., Cattani, O., Vitali, G. and Cortesi, P. (2001b) Influence of incubation conditions on the anoxic survival of marine bivalves. Static and semi-static incubations. Marine Ecology Progress Series 211, 169–179.Google Scholar
De Zwaan, A., Isani, G., Cattani, O. and Cortesi, P. (1995) Long-term anaerobic metabolism of erythrocytes of the arcid clam Scapharca inaequivalvis . Journal of Experimental Marine Biology and Ecology 187, 27–37.Google Scholar
De Zwaan, A., Schaub, B.E.M. and Babarro, J.M.F. (2001a) Anoxic survival of Macoma balthica: the effect of antibiotics, molybdate and sulphide. Journal of Experimental Marine Biology and Ecology 256, 241–251.CrossRefGoogle ScholarPubMed
Diaz, R.J. and Rosenberg, R.R. (1995) Marine benthic hypoxia: a review of its ecological effects and the behavioural responses of benthic macrofauna. Oceanography and Marine Biology: an Annual Review 33, 245–303.Google Scholar
Diaz, R.J. and Rosenberg, R.R. (2008) Spreading dead zones and consequences for marine ecosystems. Science 321, 926–929.Google Scholar
Grieshaber, M.K. and Völkel, S. (1998) Animal adaptations for tolerance and exploitation of poisonous sulfide. Annual Review of Physiology 60, 33–53.Google Scholar
Hildebrandt, T.M. and Grieshaber, M.K. (2008) Three enzymatic activities catalyze the oxidation of sulfide to thiosulfate in mammalian and invertebrate mitochondria. FEBS Journal 275, 3352–3361.Google Scholar
Hochachka, P.W. and Somero, G.N. (2002) Biochemical adaptation: mechanism and process in physical evolution. Oxford: Oxford University Press.Google Scholar
Ishii, S. (1931) Research on red tides in Lake Nakaumi. Kaiyojihou 3, 195–198. [In Japanese]Google Scholar
Kikuchi, T. (1964) Ecology and biological production of Lake Naka-umi and adjacent regions. 3. Macro-benthic communities of Lake Shinji-ko and Lake Naka-umi. Special Publications from the SETO Marine Biological Laboratory 2, 21–44.CrossRefGoogle Scholar
Kitamura, K. (1935) Nakaumi census. Hamada Meteorological Station, Shimane Prefecture, no. 1934, 1–30. [In Japanese]Google Scholar
Laudien, J., Schiedek, D., Brey, T., Pörtner, H.O. and Arntz, W.E. (2002) Survivorship of juvenile surf clams Donax serra (Bivalvia, Donacidae) exposed to severe hypoxia and hydrogen sulphide. Journal of Experimental Marine Biology and Ecology 271, 9–23.CrossRefGoogle Scholar
Levitt, J.M. and Arp, A.J. (1991) The effects of sulfide on the anaerobic metabolism of 2 congeneric species of mudflat clams. Comparative Biochemistry and Physiology, Part B 98, 339–347.Google Scholar
Lipej, L., Mavrič, B., Orlando-Bonaca, M. and Malej, A. (2012) State of the art of the marine non-indigenous flora and fauna in Slovenia. Mediterranean Marine Science 13, 243–249.Google Scholar
Marcus, N.H., Lutz, R.V. and Chanton, J.P. (1997) Impact of anoxia and sulfide on the viability of eggs of three planktonic copepods. Marine Ecology Progress Series 146, 291–295.Google Scholar
Miyamoto, Y. and Iwanaga, C. (2012) Biochemical responses to anoxia and hypoxia in the ark shell Scapharca kagoshimensis . Plankton and Benthos Research 7, 167–174.Google Scholar
Moriwaki, S. and Michine, A. (2007) Catch fluctuations in Nakaumi, estuarine inland-sea, western Japan. Bulletin of Shimane Prefectural Fisheries Experimental Station 2007, 41–48. [In Japanese]Google Scholar
Nakamura, M., Shinagawa, A., Toda, K. and Nakao, S. (1997) Tolerance of 4 bivalves from Lakes Shinji and Nakaumi to environmental factors. Aquaculture Science 45, 179–185. [In Japanese with English abstract]Google Scholar
Nicolls, P. and Kim, J.K. (1982) Sulfide as an inhibitor and electron donor for the cytochrome-c oxidase system. Canadian Journal of Biochemistry 60, 613–623.Google Scholar
Powell, M.A. and Somero, G.N. (1983) Blood components prevent sulfide poisoning of respiration of the hydrothermal vent tube worm Riftia pachyptila . Science 219, 297–299.Google Scholar
Powell, M.A. and Somero, G.N. (1986) Adaptations to sulfide by hydrothermal vent animals: sites and mechanisms of detoxification and metabolism. Biological Bulletin 171, 274–290.Google Scholar
R Development Core Team (2011) R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. Available at: http://www.R-project.org.Google Scholar
Sakai, S., Nakaya, M., Sampei, Y., Dettman, D.L. and Takayasu, K. (2013) Hydrogen sulfide and organic carbon at the sediment–water interface in coastal brackish Lake Nakaumi, SW Japan. Environmental Earth Sciences 68, 1999–2006.Google Scholar
Sakai, S., Nakaya, M. and Takayasu, K. (2004) Hydrogen sulfide distribution in bottom and pore waters during an anoxic period in Lake Nakaumi, Japan. Laguna 11, 65–68.Google Scholar
Schiedek, D., Vogan, C., Hardege, J. and Bentley, M. (1997) Marenzelleria cf. wireni (Polychaeta: Spionidae) from the Tay estuary. Metabolic response to severe hypoxia and hydrogen sulphide. Aquatic Ecology 31, 211–222.Google Scholar
Shimane Prefecture (1934) Researches on red tides in Lake Nakaumi. Bulletin of Shimane Prefectural Fisheries Experimental Station 1934, 68–83. [In Japanese]Google Scholar
Shimane Prefecture (1958) Research on mass mortality of Mogai. Bulletin of Shimane Prefectural Fisheries Experimental Station 1957–58, 259–272. [In Japanese]Google Scholar
Shumway, S.E., Scott, T.M. and Shick, J.M. (1983) The effects of anoxia and hydrogen-sulfide on survival, activity and metabolic-rate in the coot clam, Mulinia lateralis (Say). Journal of Experimental Marine Biology and Ecology 71, 135–146.CrossRefGoogle Scholar
Suzuki, H., Yamaguchi, K. and Seto, K. (2011) Growth and survival of the ark shell Scapharca kagoshimensis cultured in a semi-enclosed lagoon, Lake Nakaumi, Southwest Japan. Aquaculture Science 59, 89–99. [In Japanese with English abstract]Google Scholar
Theede, H., Ponat, A., Hiroki, K. and Schlieper, C. (1969) Studies on resistance of marine bottom invertebrates to oxygen-deficiency and hydrogen sulfide. Marine Biology 2, 325–337.Google Scholar
Uye, S., Shimazu, T., Yamamuro, M., Ishitobi, Y. and Kamiya, H. (2000) Geographical and seasonal variations in mesozooplankton abundance and biomass in relation to environmental parameters in Lake Shinji–Ohashi River–Lake Nakaumi brackish-water system, Japan. Journal of Marine Systems 26, 193–207.CrossRefGoogle Scholar
Vaquer-Sunyer, R. and Duarte, C.M. (2008) Thresholds of hypoxia for marine biodiversity. Proceedings of the National Academy of Sciences USA 105, 15452–15457.Google Scholar
Vaquer-Sunyer, R. and Duarte, C.M. (2010) Sulfide exposure accelerates hypoxia-driven mortality. Limnology and Oceanography 55, 1075–1082.Google Scholar
Vetter, R.D., Powell, M.A. and Somero, G.N. (1991) Metazoan adaptation to hydrogen sulfide. In Bryant, C. (ed.), Metazoan life without oxygen. London: Chapman and Hall, pp. 109–128.Google Scholar
Vetter, R.D., Wells, M.E., Kurtsman, A.L. and Somero, G.N. (1987) Sulfide detoxification by the hydrothermal vent crab Bythograea thermodron and other decapod crustaceans. Physiological Zoology 60, 121–137.Google Scholar
Vismann, B. (1993) Hematin and sulfide removal in hemolymph of the hemoglobin-containing bivalve Scapharca inaequivalvis . Marine Ecology Progress Series 98, 115–122.Google Scholar
Völkel, S., Auschild, K.H. and Grieshaber, M.K. (1995) Sulfide stress and tolerance in the lugworm Arenicola marina during low tide. Marine Ecology Progress Series 122, 205–215.Google Scholar
Windoffer, R., Jahn, A., Meyberg, F., Krieger, J. and Giere, O. (1999) Sulphide-induced metal precipitation in the mantle edge of Macoma balthica (Bivalvia, Tellinidae) – a means of detoxification. Marine Ecology Progress Series 187, 159–170.Google Scholar
Yurimoto, T., Mori, Y., Ito, S. and Maeno, Y. (2008) Reproductive cycle of the subcrenated ark shell Scapharca kagoshimensis (Tokunaga, 1906) in Ariake Bay, Japan. Journal of Shellfish Research 27, 1101–1108.Google Scholar