Impact of ocean acidification and warming on the feeding behaviour of two gastropod species

Published: Dec 20, 2019
Acidification Climate change Feeding Behaviour Gastropods

Increased atmospheric CO2 produced by anthropogenic activities will be absorbed by the oceans over the next century causing ocean acidification and changes in the seawater carbonate chemistry. Elevated CO2 causes sublethal physiological and behavioural responses on the locomotion and foraging behaviour of marine organisms. This study aims to investigate the independent and synergistic effects of long term exposure to low pH and increased temperature on the feeding behaviour of two gastropod species, Hexaplex trunculus and Nassarius nitidus, both in adults and juveniles. Gastropods were maintained under controlled conditions of temperature (ambient = 20°C, increased = 23°C) and pH (ambient = 8, low = 7.6) for 2.5 years. The percentage of animals which successfully reached their food, the response time until gastropods began moving, the total duration until they reached food and the total distance covered, were measured. Speed and path index (i.e how straightforward the movement is) were estimated as means of foraging efficiency. Increased temperature (under ambient pH) resulted in faster responses, a shorter duration until food was reached and a higher speed in H. trunculus adults. H. trunculus (both adults and juveniles) were less successful in reaching their food source under low pH and ambient temperature in comparison to all other treatments. The response time, duration, speed and path index were not affected by low pH (at ambient or increased temperature) for H. trunculus adults and juveniles, as well as for N. nitidus. The foraging performance of juveniles hatched and developed under low pH (either at ambient or increased temperature) was more effective than adults of the same species, thus indicating a degree of acclimation. Also, the scavenger N. nitidus was more successful and responded faster in reaching carrion than the predator H. trunculus, whereas no significant effects were observed for N. nitidus under low pH.

Article Details
  • Section
  • Special Issue MEDIAS
Download data is not yet available.
Bibby, R., Cleall-Harding, P., Rundle, S., Widdicombe, S., Spicer, J., 2007. Ocean acidification disrupts induced defences in the intertidal gastropod Littorina littorea. Biology Letters, 3, 699-701.
Chatzinikolaou, E., Grigoriou, P., Keklikoglou, K., Faulwetter, S., Papageorgiou, N., 2017. The combined effects of reduced pH and elevated temperature on the shell density of two gastropod species measured using micro-CT imaging. ICES Journal of Marine Science, 74 (4), 1135-1149.
Clements, J.C., Darrow, E.S., 2018. Eating in an acidifying ocean: a quantitative review of elevated CO2 effects on the feeding rates of calcifying marine invertebrates. Hydrobiologia, 820, 1–21.
Cramer, W., Guiot, J., Fader, M., Garrabou, J., Gattuso, J-P. et al., 2018. Climate change and interconnected risks to sustainable development in the Mediterranean. Nature Climate Change, 8, 972–980.
Crisp, M., 1971. Structure and abundance of receptors of the unspecialised external epithelium of Nassarius reticulatus Gastropoda: Prosobranchia). Journal of Marine Biological Association UK, 51, 865-890.
Crisp, M., Davenport, J., Shumway, S.E., 1978. Effects of feeding and of chemical stimulation on the oxygen uptake of Nassarius reticulatus (Gastropoda: Prosobranchia). Journal of the Marine Biological Association of the UK, 58, 387-399.
De La Haye, K.L., Spicer, J.I., Widdicombe, S., Briffa, M., 2012. Reduced pH sea water disrupts chemo-responsive behaviour in an intertidal crustacean. Journal of Experimental Marine Biology and Ecology, 412, 134–140.
Dickson, A.G., Millero, F.J., 1987. A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep-Sea Research, A34, 1733–1743.
Dlugokencky, E., 2016. Annual Mean Carbon Dioxide Data. Earth System Research Laboratory. National Oceanic and Atmospheric Administration.
Domenici, P., Torres, R., Manrı́quez, P.H., 2017. Effects of elevated carbon dioxide and temperature on locomotion and the repeatability of lateralization in a keystone marine mollusc. Journal of Experimental Biology, 220, 667-676.
Doney, S.C., Fabry, V.J., Feely, R.A., Kleypas, J.A., 2009. Ocean Acidification: The Other CO2 Problem. Annual Reviews of Marine Science, 1, 169-192.
Dorsett, D.A., 1986. Brains to cells: the neuroanatomy of selected gastropod species. In: The Mollusca : Neurobiology and Behaviour part II. Willow, A.O.D. (Ed). Academic Press Inc. 499p.
FAO, 2012. The state of world fisheries and aquaculture. FAO Fisheries and Aquaculture Department, Rome, 230pp.
Fretter, V., Graham, A., 1984. The prosobranch molluscs of Britain and Denmark. Part 8. Neogastropoda. Journal of Molluscan Studies, 15 supplement, 435-556.
Garrard, S.L., Gambi, C.M., Scipione, B.M., Patti, F.P., Lorenti, M. et al., 2014. Indirect effects may buffer negative responses of seagrass invertebrate communities to ocean acidification. Journal of Experimental Marine Biology and Ecology, 461, 31-38.
Gazeau, F., Parker, L.M., Comeau, S., Gattuso, J.P., O'Connor, W.A. et al., 2013. Impacts of ocean acidification on marine shelled molluscs. Marine Biology, 160, 2207-2245.
Gooding, R.A., Harley, C.D.G., and Tang, E., 2009. Elevated water temperature and carbon dioxide concentration increase the growth of a keystone echinoderm. Proceedings of the National Academy of Sciences, 106, 9316–9321.
Gore, R.H., 1966. Observations on the escape response in Nassarius vibex (Say), (Mollusca: Gastropoda). Bulletin of Marine Science, 16 (3), 423-434.
Harvey, B.P., Gwynn-Jones, D., Moore, P.J., 2013. Meta-analysis reveals complex marine biological responses to the interactive effects of ocean acidification and warming. Ecology and Evolution, 3(4), 1016–1030.
Hendriks, I.E., Duarte, C.M., Alvarez, M., 2010. Vulnerability of marine biodiversity to ocean acidification: a meta-analysis. Estuarine, Coastal and Shelf Science, 86, 157-164.
IPCC, 2014. Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Pachauri, R.K., Meyer, L.A. (Eds). IPCC, Geneva, Switzerland. 151 pp.
Johannesen, A., Dunn, A.M., Morrell, L.J., 2012. Olfactory cue use by three-spined sticklebacks foraging in turbid water: prey detection or prey location? Animal Behaviour, 84, 151–158.
Leduc, A.O.H.C., Kelly, J.M., Brown, G.B., 2004. Detection of conspecific alarm cues by juvenile salmonids under neutral and weakly acidic conditions: laboratory and field tests. Oecologia, 137, 318-324.
Leung, J.Y.S., Russell, B.D., Connell, S.D., Ng, J.C.Y., Lo, M.M.Y., 2015. Acid dulls the senses: impaired locomotion and foraging performance in a marine mollusc. Animal Behaviour, 106, 223-229.
Manríquez, P.H., Jara, M.E., Mardones, M.L., Torres, R., Navarro, J.M. et al., 2014. Ocean acidification affects predator avoidance behaviour but not prey detection in the early ontogeny of a keystone species. Marine Ecology Progress Series, 502: 157–167.
Mehrbach, C., Culberson, C.H., Hawley, J.E., Pytkowicz, R.M., 1973. Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnology and Oceanography, 18, 897–907.
Morton, B., Yuen, W.Y., 2000. The feeding behaviour and competition for carrion between two sympatric scavengers on a sandy shore in Hong Kong: the gastropod Nassarius festivus (Powys) and the hermit crab, Diogenes edwardsii (De Haan). Journal of Experimental Marine Biology and Ecology, 246: 1-29.
Nagelkerken, I., Munday, P.L., 2016. Animal behaviour shapes the ecological effects of ocean acidification and warming: moving from individual to community level responses. Global Change Biology, 22, 974-989.
Nienhuis, S., Palmer, A.R., Harley, C.D.G., 2010. Elevated CO2 affects shell dissolution rate but not calcification rate in a marine snail. Proceedings of the Royal Society B: Biological Sciences, 277, 2553–2558.
Parker, L.M., Ross, P.M., O'Connor, W.A., Pörtner, H.O., Scanes, E. et al., 2013. Predicting the response of molluscs to the impact of ocean acidification. Biology, 2, 651-692.
Pepin, P., Robert, D., Bouchard, C., Dower, J. F., Falardeau, M. et. al., 2014. Once upon a larva: revisiting the relationship between feeding success and growth in fish larvae. ICES Journal of Marine Science, 72, 359–373.
Queirós, A.M., Fernandes, J.A. Faulwetter, S., Nunes, J., Rastrick, S.P.S. et al., 2015. Scaling up experimental ocean acidification and warming research: from individuals to the ecosystem. Global Change Biology, 21, 130–143.
Radkte, R.L., 1983. Chemical and structural characteristics of statoliths from the short-finned squid Illex illecebrosus. Marine Biology, 76, 47-54.
Ries, J.B., Cohen, A.L., McCorkle, D.C., 2009. Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology, 37, 1131-1134.
Schaum, C.E., Batty, R., Last, K.S., 2013. Smelling Danger-Alarm cue responses in the Polychaete Nereis (Hediste) diversicolor (Muller, 1776) to potential fish predation. PLoS ONE, 8, e77431.
Shirayama, Y., Thornton, H., 2005. Effect of increased atmospheric CO2 on shallow water marine benthos. Journal of Geophysical Research, 110, C09S08.
Thomsen, J., Casties, I., Pansch, C., Körtzinger, A., Melzner, F., 2013. Food availability outweighs ocean acidification effects in juvenile Mytilus edulis: laboratory and field experiments. Global Change Biology, 19, 1017–1027.
Wahl, M., Saderne, V., Sawall, Y., 2016. How good are we at assessing the impact of ocean acidification in coastal systems? Limitations, omissions and strengths of commonly used experimental approaches with special emphasis on the neglected role of fluctuations. Marine and Freshwater Research, 67, 25–36.
Watson, S.A., Lefevre, S., McCormick, M.I., Domenici, P., Nilsson, G.E., Munday, P.L., 2014. Marine mollusc predator-escape behaviour altered by near-future carbon dioxide levels. Proceedings of Royal Society B, 281(1774), 20132377.
Wright, J.M., Parker, L.M., O’Connor, W.A., Scanes, E., Ross, P.M.. 2018. Ocean acidification affects both the predator and prey to alter interactions between the oyster Crassostrea gigas (Thunberg, 1793) and the whelk Tenguella marginalba (Blainville, 1832). Marine Biology, 165, 46.
Most read articles by the same author(s)