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Parasitic infection alters the physiological response of a marine gastropod to ocean acidification

Published online by Cambridge University Press:  25 May 2016

C. D. MACLEOD  and
R. POULIN
C. D. MACLEOD*
Affiliation:
Department of Zoology, University of Otago, PO Box 56, Dunedin 9054, New Zealand
R. POULIN
Affiliation:
Department of Zoology, University of Otago, PO Box 56, Dunedin 9054, New Zealand
*
*Corresponding author. Department of Zoology, University of Otago, PO Box 56, Dunedin 9054, New Zealand. Tel: +64 3 479 7964. Fax: +64 3 479 7584. E-mail: [email protected]
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Summary

Increased hydrogen ion concentration and decreased carbonate ion concentration in seawater are the most physiologically relevant consequences of ocean acidification (OA). Changes to either chemical species may increase the metabolic cost of physiological processes in marine organisms, and reduce the energy available for growth, reproduction and survival. Parasitic infection also increases the energetic demands experienced by marine organisms, and may reduce host tolerance to stressors associated with OA. This study assessed the combined metabolic effects of parasitic infection and OA on an intertidal gastropod, Zeacumantus subcarinatus. Oxygen consumption rates and tissue glucose content were recorded in snails infected with one of three trematode parasites, and an uninfected control group, maintained in acidified (7·6 and 7·4 pH) or unmodified (8·1 pH) seawater. Exposure to acidified seawater significantly altered the oxygen consumption rates and tissue glucose content of infected and uninfected snails, and there were clear differences in the magnitude of these changes between snails infected with different species of trematode. These results indicate that the combined effects of OA and parasitic infection significantly alter the energy requirements of Z. subcarinatus, and that the species of the infecting parasite may play an important role in determining the tolerance of marine gastropods to OA.

Keywords

ocean acidificationparasitegastropodmetabolismoxygenglucose
Type
Research Article
Information
Parasitology , Volume 143 , Issue 11 , September 2016 , pp. 1397 - 1408
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Copyright
Copyright © Cambridge University Press 2016 

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References

REFERENCES

Bates, A. E., Leiterer, F., Wiedeback, M. L. and Poulin, R. (2011). Parasitized snails take the heat: a case of host manipulation? Oecologia 167, 613–621.CrossRefGoogle Scholar
Bates, D., Maechler, M., Bolker, B. and Walker, S. (2014). lme4: Linear mixed-effects models using Eigen and S4. R package version 1.1-7. http://CRAN.R-project.org/package=lme4 Google Scholar
Berthelin, C., Kellner, K. and Mathieu, M. (2000). Histological characterization and glucose incorporation into glycogen of the Pacific oyster Crassostrea gigas storage cells. Marine Biotechnology 2, 136–145.CrossRefGoogle ScholarPubMed
Cheng, T. C. (1963). Biochemical requirements of larval trematodes. Annals of the New York Academy of Sciences 113, 289–321.CrossRefGoogle ScholarPubMed
Cheng, T. C. and Snyder, R. W. (1963). Studies on host-parasite relationships between larval trematodes and their hosts. IV. A histochemical determination of glucose and its role in the metabolism of molluscan host and parasite. Transactions of the American Microscopical Society 82, 343–346.CrossRefGoogle Scholar
Coleman, D., Byrne, M. and Davis, A. (2014). Molluscs on acid: gastropod shell repair and strength in acidifying oceans. Marine Ecology Progress Series 509, 203–211.CrossRefGoogle Scholar
Dickson, A. G., Sabine, C. L. and Christian, J. R. (2007). Guide to best practices for ocean CO2 measurements. PICES Special Publication 3 191, 1–176.Google Scholar
Ellis, R., Bersey, J., Rundle, S., Hall-Spencer, J. and Spicer, J. (2009). Subtle but significant effects of CO2 acidified seawater on embryos of the intertidal snail, Littorina obtusata . Aquatic Biology 5, 41–48.CrossRefGoogle Scholar
Fox, J., Weisburg, S., Adler, D., Bates, D., Baud-Bovy, G., Ellison, S., Firth, D., Friendly, M., Gorjanc, G., Graves, S., Heiburger, R., Laboissiere, R., Monette, G., Murdoch, D., Nilsson, H., Ripley, B., Venables, W. and Zeileis, A. (2014). Companion to applied regression. https://r-forge.r-project.org/projects/car/ Google Scholar
Fredensborg, B. L., Mouritsen, K. N. and Poulin, R. (2005). Impact of trematodes on host survival and population density in the intertidal gastropod Zeacumantus subcarinatus . Marine Ecology Progress Series 290, 109–117.CrossRefGoogle Scholar
Fried, B. and Graczyk, T. K. (1997). Advances in Trematode Biology. CRC Press, Boca Raton, FL.Google Scholar
Galaktionov, K. V. and Dobrovolskij, A. A. (2003). The Biology of Trematodes. Kluwer, Dordrecht.CrossRefGoogle Scholar
Graham, A. L. (2003). Effects of snail size and age on the prevalence and intensity of avian schistosome infection: relating laboratory to field studies. Journal of Parasitology 89, 458–463. doi: http://dx.doi.org/10.1645/0022-3395(2003)089[0458:EOSSAA]2.0.CO;2 CrossRefGoogle ScholarPubMed
Hay, K. B., Fredensborg, B. L. and Poulin, R. (2005). Trematode-induced alterations in shell shape of the mud snail Zeacumantus subcarinatus (Prosobranchia: Batillariidae). Journal of the Marine Biological Association of the United Kingdom 85, 989–992. doi: http://dx.doi.org/10.1017/S0025315405012002 CrossRefGoogle Scholar
Hochachka, P. W. (1983). Mollusca: Metabolic Biochemistry and Molecular Biomechanics. Academic Press, London.Google Scholar
Hunter, K. A. (2007). SWCO2 Seawater CO2 Equilibrium Calculations, University of Otago, New Zealand. http://neon.otago.ac.nz/research/mfc/people/keith_hunter/software/swco2/ Google Scholar
IPCC (2014). Summary for policymakers. In: Climate Change 2014: Impacts, Adaptation, and Vulnerability. Part A: Global and Sectoral Aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (eds Field, C. B., Barros, V. R., Dokken, D. J., Mach, K. J., Mastrandrea, M. D., Bilir, T. E., Chatterjee, M., Ebi, K. L., Estrada, Y. O., Genova, R. C., Girma, B., Kissel, E. S., Levy, A. N., MacCracken, S., Mastrandrea, P. R. and White, L. L.), pp. 1–32. Cambridge University Press, Cambridge, UK and New York, NY, USA.Google Scholar
Kelly, M. W. and Hofmann, G. E. (2013). Adaptation and the physiology of ocean acidification. Functional Ecology 27, 980–990.CrossRefGoogle Scholar
Kimura, R., Takami, H., Ono, T., Onitsuka, T. and Nojiri, Y. (2011). Effects of elevated pCO2 on the early development of the commercially important gastropod, Ezo abalone Haliotis discus hannai: effects of high pCO2 on larval Ezo abalone. Fisheries Oceanography 20, 357–366.CrossRefGoogle Scholar
Lacoste, A., Jalabert, F., Malham, S. K., Cueff, A. and Poulet, S. A. (2001). Stress and stress-induced neuroendocrine changes increase the susceptibility of juvenile oysters (Crassostrea gigas) to Vibrio splendidus . Applied and Environmental Microbiology 67, 2304–2309.CrossRefGoogle ScholarPubMed
Lardies, M. A., Arias, M. B., Poupin, M. J., Manríquez, P. H., Torres, R., Vargas, C. A., Navarro, J. M. and Lagos, N. A. (2014). Differential response to ocean acidification in physiological traits of Concholepas concholepas populations. Journal of Sea Research 90, 127–134.CrossRefGoogle Scholar
Leung, T. L. F., Donald, K. M., Keeney, D. B., Koehler, A. V., Peoples, R. C. and Poulin, R. (2009). Trematode parasites of Otago Harbour (New Zealand) soft-sediment intertidal ecosystems: life cycles, ecological roles and DNA barcodes. New Zealand Journal of Marine and Freshwater Research 43, 857–865.CrossRefGoogle Scholar
MacLeod, C. D. (2015). The effects of ocean acidification on host-parasite associations. PhD thesis. University of Otago, New Zealand.Google Scholar
MacLeod, C. D. and Poulin, R. (2015). Interactive effects of parasitic infection and ocean acidification on the calcification of a marine gastropod. Marine Ecology – Progress Series 537, 137–150.CrossRefGoogle Scholar
MacLeod, C. D., Doyle, H. L. and Currie, K. I. (2015). Technical note: maximising accuracy and minimising cost of a potentiometrically regulated ocean acidification simulation system. Biogeosciences 12, 713–721.CrossRefGoogle Scholar
Macnab, V. and Barber, I. (2012). Some (worms) like it hot: fish parasites grow faster in warmer water, and alter host thermal preferences. Global Change Biology 18, 1540–1548.CrossRefGoogle Scholar
Martínez-Quintana, J. A. and Yepiz-Plascencia, G. (2012). Glucose and other hexoses transporters in marine invertebrates: a mini review. Electronic Journal of Biotechnology 15, 1–12.Google Scholar
Martorelli, S. R., Fredensborg, B. L., Mouritsen, K. N. and Poulin, R. (2004). Description and proposed life cycle of Maritrema novaezealandensis n. sp.(Microphallidae) parasitic in red-billed gulls, Larus novaehollandiae scopulinus, from Otago Harbor, South Island, New Zealand. Journal of Parasitology 90, 272–277.CrossRefGoogle Scholar
Martorelli, S. R., Fredensborg, B. L., Leung, T. L. F. and Poulin, R. (2008). Four trematode cercariae from the New Zealand intertidal snail Zeacumantus subcarinatus (Batillariidae). New Zealand Journal of Zoology 35, 73–84.CrossRefGoogle Scholar
McDaniel, J. S. and Dixon, K. E. (1967). Utilization of exogenous glucose by the rediae of Parorchis acanthus (Digenea: Philophthalmidae) and Cryptocotyle lingua (Digenea: Heterophyidae). Biological Bulletin 133, 591–599.CrossRefGoogle ScholarPubMed
Melatunan, S., Calosi, P., Rundle, S. D., Moody, A. J. and Widdicombe, S. (2011). Exposure to elevated temperature and pCO2 reduces respiration rate and energy status in the periwinkle Littorina littorea . Physiological and Biochemical Zoology 84, 583–594.CrossRefGoogle ScholarPubMed
Pan, T.-C. F., Applebaum, S. L. and Manahan, D. T. (2015). Experimental ocean acidification alters the allocation of metabolic energy. Proceedings of the National Academy of Sciences of the United States of America 112, 4696–4701.CrossRefGoogle ScholarPubMed
Parker, L., Ross, P., O'Connor, W., Pörtner, H., Scanes, E. and Wright, J. (2013). Predicting the response of molluscs to the impact of ocean acidification. Biology 2, 651–692.CrossRefGoogle Scholar
Pojmanska, T. and Machaj, K. (1991). Differentiation of the ultrastructure of the body wall of the sporocyst of Leucochloridwm paradoxum . International Journal for Parasitology 21, 651–659.CrossRefGoogle Scholar
Popiel, I. and James, B. L. (1976). The effect of glycogen and glucose on oxygen consumption in the daughter sporocysts of Cercaria linearis stunkard, 1932 and Cercaria stunkardi palombi, 1934 (Digenea: Opecoelidae). Zeitschrift für Parasitenkunde 51, 71–77.CrossRefGoogle Scholar
Pörtner, H. (2008). Ecosystem effects of ocean acidification in times of ocean warming: a physiologist's view. Marine Ecology Progress Series 373, 203–217.CrossRefGoogle Scholar
Pörtner, H. O. and Farrell, A. P. (2008). Physiology and climate change. Science 322, 690–692.CrossRefGoogle ScholarPubMed
Pörtner, H. O., Bock, C. and Reipschlager, A. (2000). Modulation of the cost of pHi regulation during metabolic depression: a (31) P-NMR study in invertebrate (Sipunculus nudus) isolated muscle. Journal of Experimental Biology 203, 2417–2428.CrossRefGoogle Scholar
R Development Core Team (2014). R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing, Vienna, Austria, ISBN 3-900051-07-0.Google Scholar
Richards, R. J. (1970). Variations in the oxygen uptake, reduced weight and metabolic rate of starving sporocysts of Microphallus pygmaeus (Levinsen, 1881)(Trematoda: Microphallidae). Journal of Helminthology 44, 75–88.CrossRefGoogle Scholar
Richards, R. J., Pascoe, D. and James, B. L. (1972). Variations in the metabolism of the daughter sporocysts of Microphallus pygmaeus in a chemically defined medium. Journal of Helminthology 46, 107–116.CrossRefGoogle Scholar
Sorensen, R. E. and Minchella, D. J. (2001). Snail–trematode life history interactions: past trends and future directions. Parasitology 123, S3–S18.CrossRefGoogle ScholarPubMed
Toledo, R. and Fried, B. eds. (2011). Biomphalaria Snails and Larval Trematodes. Springer New York, New York, NY.CrossRefGoogle Scholar
Van Hellemond, J. J., Van Remoortere, A. and Tielens, A. G. M. (1997). Schistosoma mansoni sporocysts contain rhodoquinone and produce succinate by fumarate reduction. Parasitology 115, 177–182.CrossRefGoogle ScholarPubMed
Vernberg, W. B. (1963). Respiration of digenetic trematodes. Annals of the New York Academy of Sciences 113, 261–271.CrossRefGoogle ScholarPubMed
Zhang, H., Cheung, S. G. and Shin, P. K. S. (2014). The larvae of congeneric gastropods showed differential responses to the combined effects of ocean acidification, temperature and salinity. Marine Pollution Bulletin 79, 39–46.CrossRefGoogle Scholar
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