Larval development of the barnacle Amphibalanus improvisus responds variably but robustly to near-future ocean acidification

ICES Journal of Marine Science

Volumn 70, Issue 4, 2013, Pages 805-811

  Pansch, Christian ^a   Schlegel, Peter ^b   Havenhand, Jonathan ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b MACQUARIE UNIVERSITY   (Australia)

Author keywords

Amphibalanus (balanus) improvisus; barnacle; Co2; cyprids; development; early life history; larvae; nauplii; ocean acidification; ph

Indexed keywords

ACIDIFICATION; CARBON DIOXIDE; CRUSTACEAN; GENETIC VARIATION; LARVAL DEVELOPMENT; LIFE HISTORY; PH; SEAWATER;

EID: 84880361571     PISSN: 10543139     EISSN: 10959289     Source Type: Journal    
DOI: 10.1093/icesjms/fst092     Document Type: Article

References (51)

1. Andersson, M., Berggren, M., Wilhelmsson, D., andÖ hman, M. 2009. Epibenthic colonization of concrete and steel pilings in a coldtemperate embayment: a field experiment. Helgoland Marine Research, 63: 249-260.
2. Andersson, M., Berntsson, K., Jonsson, P., and Gatenholm, P. 1999. Microtextured surfaces: towards macrofouling resistant coatings. Biofouling, 14: 167-178.
3. Arnold, K. E., Findlay, H. S., Spicer, J. I., Daniels, C. L., and Boothroyd, D. 2009. Effect of CO2-related acidification on aspects of the larval development of the European lobster, Homarus gammarus (L.). Biogeosciences, 6: 1747-1754.
4. Beckerman, A. P., Benton, T. G., Ranta, E., Kaitala, V., and Lundberg, P. 2002. Population dynamic consequences of delayed life-history effects. Trends in Ecology & Evolution, 17: 263-269.
5. Blackford, J. C., andGilbert, F. J. 2007. pHvariability andCO2 induced acidification in the North Sea. Journal of Marine Systems, 64: 229-241.
6. Byrne, M. 2012. Global change ecotoxicology: Identification of early life history bottlenecks in marine invertebrates, variable species responses and variable experimental approaches. Marine Environmental Research, 76: 3-15.
7. Caldeira, K., and Wickett, M. E. 2005. Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. Journal of Geophysical Research, 110: C09S04.
8. Dupont, S., Havenhand, J., Thorndyke,W., Peck, L., and Thorndyke, M. 2008. Near-future level of CO2-driven ocean acidification radically affects larval survival and development in the brittlestar Ophiothrix fragilis. Marine Ecology Progress Series, 373: 285-294.
9. Egilsdottir, H., Spicer, J. I., and Rundle, S. D. 2009. The effect of CO2 acidified sea water and reduced salinity on aspects of the embryonic development of the amphipod Echinogammarus marinus (Leach). Marine Pollution Bulletin, 58: 1187-1191.
10. Feely,R.A.,Alin, S. R.,Newton, J., Sabine,C.L.,Warner,M.,Devol, A., Krembs, C., et al. 2010. The combined effects of ocean acidification, mixing, and respiration on pH and carbonate saturation in an urbanized estuary. Estuarine Coastal and Shelf Science, 88: 442-449.
11. Findlay, H. S., Kendall, M. A., Spicer, J. I., and Widdicombe, S. 2009. Future high CO2 in the intertidal may compromise adult barnacle Semibalanus balanoides survival and embryonic development rate. Marine Ecology Progress Series, 389: 193-202.
12. Frommel, A. Y., Maneja, R., Lowe, D., Malzahn, A. M., Geffen, A. J., Folkvord, A., Piatkowski, U., et al. 2012. Severe tissue damage in Atlantic cod larvae under increasing ocean acidification. Nature Climate Change, 2: 42-46.
13. Gohad, N. V., Dickinson, G. H., Orihuela, B., Rittschof, D., and Mount, A. S. 2009. Visualization of putative ion-transporting epithelia in Amphibalanus amphitrite using correlative microscopy: Potential function in osmoregulation and biomineralization. Journal of Experimental Marine Biology and Ecology, 380: 88-98.
14. Hale, R., Calosi, P.,McNeill, L., Mieszkowska, N., andWiddicombe, S. 2011. Predicted levels of future ocean acidification and temperature rise could alter community structure and biodiversity in marine benthic communities. Oikos, 120: 661-674.
15. Harvey, B. P., Gwynn-Jones, D., and Moore, P. J. 2013. Meta-analysis reveals complex marine biological responses to the interactive effects of ocean acidification and warming. Ecology and Evolution, 3: 1016-1030.
16. Havenhand, J. N., Dupont, S., and Quinn, G. P. 2010. Designing ocean acidification experiments to maximise inference. In Guide to Best Practices for Ocean Acidification Research and Data Reporting, pp. 67-80. Ed. by U. Riebesell, V. J. Fabry, L. Hansson, and J. P. Gattuso. Publications Office of the European Union Luxembourg.
17. Gattuso. Publications Office of the European Union, Luxembourg. Hedges, L. V., Gurevitch, J., and Curtis, P. S. 1999. The meta-analysis of response ratios in experimental ecology. Ecology, 80: 1150-1156.
18. Jarrett, J. N., and Pechenik, J. A. 1997. Temporal variation in cyprid quality and juvenile growth capacity for an intertidal barnacle. Ecology, 78: 1262-1265.
19. Jones, L. W. G., and Crisp, D. J. 1954. The larval stages of the barnacle Balanus improvisus Darwin. Proceedings of the Zoological Society of London, 123: 765-780.
20. Kroeker,K. J.,Kordas, R. L., Crim, R., Hendriks, I. E., Ramajo, L., Singh, G. S., Duarte, C. M., et al. 2013. Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Global Change Biology, 19: 1884-1896.
21. Kroeker, K. J., Kordas, R. L., Crim, R. N., and Singh, G. G. 2010. Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecology Letters, 13: 1419-1434.
22. Kurihara, H. 2008. Effects ofCO2-driven ocean acidificationon the early developmental stages of invertebrates. Marine Ecology Progress Series, 373: 275-284.
23. Kurihara, H., Asai, T., Kato, S., and Ishimatsu, A. 2009. Effects of elevated pCO(2) on early development in the mussel Mytilus galloprovincialis. Aquatic Biology, 4: 225-233.
24. Kurihara, H., Kato, S., and Ishimatsu, A. 2007. Effects of increased seawater pCO2 on early development of the oyster Crassostrea gigas. Aquatic Biology, 1: 91-98.
25. Kurihara, H., Shimode, S., and Shirayama, Y. 2004. Effects of raisedCO2 concentration on the egg production rate and early development of two marine copepods (Acartia steueri andAcartia erythraea). Marine Pollution Bulletin, 49: 721-727.
26. McDonald, M. R., McClintock, J. B., Amsler, C. D., Rittschof, D., Angus, R. A., Orihuela, B., and Lutostanski, K. 2009. Effects of ocean acidification over the life history of the barnacle Amphibalanus amphitrite. Marine Ecology Progress Series, 385: 179-187.
27. Miller, A. W., Reynolds, A. C., Sobrino, C., and Riedel, G. F. 2009. Shellfish face uncertain future in high CO2 world: influence of acidification on oyster larvae calcification and growth in estuaries. PLOS ONE, 4: e5661.
28. Nakagawa, S., and Cuthill, I. C. 2007. Effect size, confidence interval and statistical significance: a practical guide for biologists. Biological Reviews, 82: 591-605.
29. Nasrolahi, A., Sari, A., Saifabadi, S., and Malek, M. 2007. Effects of algal diet on larval survival and growth of the barnacle Amphibalanus (Balanus) improvisus. Journal of the Marine Biological Association of the United Kingdom, 87: 1227-1233.
30. Pansch, C., Nasrolahi, A., Appelhans,Y. S., andWahl, M.2012a. Impacts of ocean warming and acidification on the larval development of the barnacle Amphibalanus improvisus. Journal of Experimental Marine Biology and Ecology, 420-421: 48-55.
31. Pansch, C., Nasrolahi, A., Appelhans, Y. S., and Wahl, M. 2012b. Tolerance of juvenile barnacles (Amphibalanus improvisus) to warming and elevated pCO2. Marine Biology, 1-13.
32. Parker, L. M., Ross, P. M., and O'Connor,W.A. 2011. Populations of the Sydney rock oyster, Saccostrea glomerata, vary in response to ocean acidification. Marine Biology, 158: 689-697.
33. Pechenik, J. A.,Wendt, D. E., and Jarrett, J. N. 1998. Metamorphosis is not a new beginning. Bioscience, 48: 901-910.
34. Pitombo, F. B. 2004. Phylogenetic analysis of the Balanidae (Cirripedia, Balanomorpha). Zoologica Scripta, 33: 261-276.
35. Ross, P. M., Parker, L., O'Connor, W. A., and Bailey, E. A. 2011. The impact of ocean acidification on reproduction, early development and settlement of marine organisms.Water, 3: 1005-1030.
36. Salisbury, J., Green, M., Hunt, C., and Campbell, J. 2008. Coastal acidification by rivers: A threat to shellfish? Eos, Transactions American Geophysical Union, 89: 513.
37. Schlegel, P., Havenhand, J. N., Gillings, M. R., and Williamson, J. E. 2012. Individual variability in reproductive success determines winners and losers under ocean acidification: a case study with sea urchins. PLOS ONE, 7: e53118.
38. Semmler, H., Hoeg, J. T., Scholtz, G., and Wanninger, A. 2009. Three-dimensional reconstruction of the naupliar musculature and a scanning electron microscopy atlas of nauplius development of Balanus improvisus (Crustacea: Cirripedia: Thoracica). Arthropod Structure & Development, 38: 135-145.
39. Shim, J., Kim,D.,Kang, Y. C., Lee, J. H., Jang, S. T., and Kim, C. H. 2007. Seasonal variations in pCO2 and its controlling factors in surface seawater of the northern East China Sea. Continental Shelf Research, 27: 2623-2636.
40. Strathmann, M. F. 1987. Reproduction and Development of Marine Invertebrates of the Northern Pacific coast. University of Washington Press, Seattle and London.
41. Sunday, J. M., Crim, R. N., Harley, C. D. G., and Hart, M. W. 2011. Quantifying rates of evolutionary adaptation in response to ocean acidification. PLOS ONE, 6: e22881.
42. Thiyagarajan, V., Harder, T., and Qian, P. Y. 2002. Effect of the physiological condition of cyprids and laboratory-mimicked seasonal conditions on the metamorphic successes of Balanus amphitrite Darwin (Cirripedia; Thoracica). Journal of Experimental Marine Biology and Ecology, 274: 65-74.
43. Thiyagarajan, V., Harder, T., Qiu, J. W., and Qian, P. Y. 2003. Energy content at metamorphosis and growth rate of the early juvenile barnacle Balanus amphitrite. Marine Biology, 143: 543-554.
44. Thomsen, J., Casties, I., Pansch, C.,Körtzinger, A., and Melzner, F. 2013. Food availability outweighs ocean acidification effects in juvenile Mytilus edulis: laboratory and field experiments. Global Change Biology, 19: 1017-1027.
45. Thomsen, J.,Gutowska, M., Saphörster, J.,Heinemann, A.,Trübenbach, K., Fietzke, J., Hiebenthal, C., et al. 2010. Calcifying invertebrates succeed in a naturally CO2-rich coastal habitat but are threatened by high levels of future acidification. Biogeosciences, 7: 3879-3891.
46. Underwood, A. 1997. Experiments in Ecology. Cambridge University Press, Cambridge.
47. Wakefield, R. L., andMurray, S. N. 1998. Factors influencing food choice by the seaweed-eating marine snail Norrisia norrisi (Trochidae). Marine Biology, 130: 631-642.
48. Walther, K., Anger, K., and Pörtner,H.O. 2010. Effects of ocean acidification and warming on the larval development of the spider crab Hyas araneus from different latitudes (54 degrees vs. 79 degrees N). Marine Ecology Progress Series, 417: 159-170.
49. West,T. L., and Costlow, J.D. 1987. Size regulation in larvae of the crustacean Balanus eburneus (Cirripedia, Thoracica). Marine Biology, 96: 47-58.
50. Whiteley, N.M. 2011. Physiological and ecological responses of crustaceans to ocean acidification. Marine Ecology Progress Series, 430: 257-271.
51. Wootton, J. T., Pfister, C. A., and Forester, J.D. 2008. Dynamic patterns and ecological impacts of declining ocean pH in a high-resolution multi-year dataset. Proceedings of the National Academy of Sciences of the United States of America, 105: 18848-18853.