Effects of ocean-acidification-induced morphological changes on larval swimming and feeding

Journal of Experimental Biology

Volumn 214, Issue 22, 2011, Pages 3857-3867

  Chan, Kit Yu Karen ^a   Grünbaum, Daniel ^a   O'Donnell, Michael J ^b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Biomechanics; Functional morphology; Invertebrate larvae; Ocean acidification; Sublethal effect; Swimming performance

Indexed keywords

ACID; CARBON DIOXIDE; SEA WATER;

ANIMAL; ARTICLE; CHEMISTRY; FEEDING BEHAVIOR; HISTOLOGY; LARVA; METABOLISM; PH; PHYSIOLOGY; SEA; SEA URCHIN; SWIMMING;

ACIDS; ANIMALS; CARBON DIOXIDE; FEEDING BEHAVIOR; HYDROGEN-ION CONCENTRATION; LARVA; OCEANS AND SEAS; SEA URCHINS; SEAWATER; SWIMMING;

CLYPEASTEROIDA; DENDRASTER EXCENTRICUS; INVERTEBRATA;

EID: 80054991144     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.054809     Document Type: Article

References (58)

1. Abramoff, M. D., Magelhaes, P. J. and Ram, S. J. (2004). Image processing with ImageJ. Biophotonics Int. 11, 36-42.
2. Boidron-Metairon, I. F. (1988). Morphological plasticity in laboratory-reared echinoplutei of Dendraster excentricus (Eschscholtz) and Lytechinus variegatus (Lamarck) in response to food conditions. J. Exp. Mar. Biol. Ecol. 119, 31-41. (Pubitemid 19321543)
3. Bertram, D. F. and Strathmann, R. R. (1998). Effects of maternal and larval nutrition on growth and form of planktotrophic larvae. Ecology 79, 315-327. (Pubitemid 28397849)
4. 2 ocean across a range of sperm densities. Mar. Environ. Res. 69, 234-239.
5. Caldeira, K. and Wickett, M. E. (2003). Anthropogenic carbon and ocean pH. Nature 425, 365. (Pubitemid 37187256)
6. Chan, K. Y. K. and Grünbaum, D. (2010). Effects of temperature and diet on larval swimming behaviors of sand dollar Dendraster excentricus. Mar. Ecol. Prog. Ser. 415, 49-59.
7. Chia, F. S., Buckland-Nicks, J., Young, C. M., Brodsky, L. M., Weatherhead, P. J., Turner, J. C., Staaland, H., Jacobsen, E., White, R. G. and Keast, A. (1984). Locomotion of marine invertebrate larvae: a review. Can. J. Zool. 62, 1205-1222. (Pubitemid 16271610)
8. Clark, D., Lamare, M. and Barker, M. (2009). Response of sea urchin pluteus larvae (Echinodermata: Echinoidea) to reduced seawater pH: a comparison among a tropical, temperate, and a polar species. Mar. Biol. 156, 1125-1137.
9. Clay, T. W. and Grünbaum, D. (2010). Morphology-flow interactions lead to stageselective vertical transport of larval sand dollars in shear flow. J. Exp. Biol. 213, 1281-1292.
10. Clay, T. W. and Grünbaum, D. (2011). Swimming performance as contraint on larval morphology in plutei. Mar. Ecol. Prog. Ser. 423, 185-196.
11. Cowen, R. K., Lwiza, K. M. M., Sponaugle, S., Paris, C. B. and Olson, D. B. (2000). Connectivity of marine populations: open or closed? Science 287, 857-859. (Pubitemid 30084329)
12. Davis, J. P. and Stephens, G. C. (1984). Uptake of free amino acids by bacteria-free larvae of the sand dollar Dendraster excentricus. Am. J. Physiol. Regul. Integr. Comp. Physiol. 247, R733-R739.
13. Decker, G. L. and Lennarz, W. J. (1988). Skeletogenesis in the sea urchin embryo. Development 103, 231-247.
14. 2 Measurements. PICES Special Publication 3, 191 pp.
15. 2 problem. Annu. Rev. Mar. Sci. 1, 169-192.
16. 2-driven ocean acidification on invertebrates'early life history: what we know, what we need to know and what we can do. Biogeosci. Disc. 6, 3109-3131.
17. 2-driven ocean acidification radically affects larval survival and development in the brittlestar Ophiothrix fragilis. Mar. Ecol. Prog. Ser. 373, 285-294.
18. Emlet, R. B. (1990). Flow fields around ciliated larvae: effects of natural and artificial tethers. Mar. Ecol. Prog. Ser. 63, 211-225.
19. Emlet, R. B. (1991). Functional constraints on the evolution of larval forms of marine invertebrates: experimental and comparative evidence. Am. Zool. 31, 707-725.
20. Evans, J. P. and Marshall, D. J. (2005). Male-by-female interactions influence fertilization success and mediate the benefits of polyandry in the sea urchin Heliocidaris erythrogramma. Evolution 59, 106-112. (Pubitemid 40181303)
21. Fabry, V. J., Seibel, B. A., Feely, R. A. and Orr, J. C. (2008). Impacts of ocean acidification on marine fauna and ecosystem processes. ICES J. Mar. Sci. 65, 414-432. (Pubitemid 351774758)
22. Feely, R. A., Sabine, C. L., Hernandez-Ayon, J. M., Ianson, D. and Hales, B. (2008). Evidence for upwelling of corrosive "acidified" water onto the continental shelf. Science 320, 1490-1492. (Pubitemid 351929427)
23. Gaines, S. and Roughgarden, J. (1985). Larval settlement rate: a leading determinant of structure in an ecological community of the marine intertidal zone. Proc. Natl. Acad. Sci. USA 82, 3707-3711.
24. 2 on shellfish calcification. Geophys. Res. Lett. 34, L07603.
25. Grünbaum, D. and Strathmann, R. R. (2003). Form, performance and trade-offs in swimming and stability of armed larvae. J. Mar. Res. 61, 659-691. (Pubitemid 38285821)
26. Hall-Spencer, J. M., Rodolfo-Metalpa, R., Martin, S., Ransome, E., Fine, M., Turner, S. M., Rowley, S. J., Tedesco, D. and Buia, M. C. (2008). Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454, 96-99. (Pubitemid 351931977)
27. Harris, R. J. (1975). A primer of multivariate statistics. Mahwah, NJ: Lawrence Erlbaum Associates.
28. 2+ inhibits particle capture by planktotrophic echinoderm larvae. Can. J. Zool. 68, 2610-2615.
29. Hart, M. W. (1991). Particle captures and the method of suspension feeding by echinoderm larvae. Biol. Bull. 180, 12-27.
30. Hart, M. W. and Strathmann, R. R. (1994). Functional consequences of phenotypic plasticity in echinoid larvae. Biol. Bull. 186, 291-312.
31. Havenhand, J. N., Buttler, F. R., Thorndyke, M. C. and Williamson, J. E. (2008). Near-future levels of ocean acidification reduce fertilization success in a sea urchin. Curr. Biol. 18, R651-R652.
32. Heyland, A. and Hodin, J. (2004). Heterochronic developmental shift caused by thyroid hormone in larval sand dollars and its implication fo phenotypic plasticity and the evolution of non-feeding development. Evolution 58, 524-538. (Pubitemid 38449128)
33. IPCC (2007). for policymakers. In Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (ed. S. Solomon), pp. 1-18. IPCC.
34. 2-driven ocean acidification on the early developmental stages of invertebrates. Mar. Ecol. Prog. Ser. 373, 275-284.
35. 2 on sea urchin early development. Mar. Ecol. Prog. Ser. 274, 161-169. (Pubitemid 38927590)
36. Langdon, C., Takahashi, T., Sweeney, C., Chipman, D., Goddard, J., Marubini, F., Aceves, H., Barnett, H. and Atkinson, M. J. (2000). Effect of calcium carbonate saturation state on the calcification rate of an experimental coral reef. Global Biogeochem. Cycles 14, 639-654.
37. Metaxas, A. (2001). Behaviour in flow: perspectives on the distribution and dispersion of meroplanktonic larvae in the water column. Can. J. Fish. Aquat. Sci. 58, 86-98. (Pubitemid 32185265)
38. Miner, B. G. (2005). Evolution of feeding structure plasticity in marine invertebrate larvae: a possible trade-off between arm length and stomach size. J. Exp. Mar. Biol. Ecol. 315, 117-125 (Pubitemid 40191533)
39. North, E. W., Schlag, Z., Hood, R. R., Li, M., Zhong, L., Gross, T. and Kennedy, V. S. (2008). Vertical swimming behavior influences the dispersal of simulated oyster larvae in a coupled particle-tracking and hydrodynamic model of Chesapeake Bay. Mar. Ecol. Prog. Ser. 359, 99-115. (Pubitemid 351798231)
40. O'Donnell, M. J., Todgham, A. E., Sewell, M. A., Hammond, L. T. M., Ruggiero, K., Fangue, N. A., Zippay, M. L. and Hofmann, G. E. (2010). Ocean acidification alters skeletogenesis and gene expression in larval sea urchins. Mar. Ecol. Prog. Ser. 398, 157-171.
41. Orr, J. C., Fabry, V. J., Aumont, O., Bopp, L., Doney, S. C., Feely, R. A., Gnanadesikan, A., Gruber, N., Ishida, A. and Joos, F. (2005). Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437, 681-686. (Pubitemid 41486531)
42. Pechenik, J. A., Wendt, D. E. and Jarrett, J. N. (1998). Metamorphosis is not a new beginning. Bioscience 48, 901-910.
43. Pennington, J. T. and Strathmann, R. R. (1990). Consequences of the calcite skeletons of planktonic echinoderm larvae for orientation, swimming, and shape. Biol. Bull. Mar. Biol. 179, 121-133.
44. Podolsky, R. D. and Emlet, R. B. (1993). Separating the effects of temperature and viscosity on swimming and water movement by sand dollar larvae (Dendraster excentricus). J. Exp. Biol. 176, 207-221.
45. Pörtner, H. O. (2008). Ecosystem effects of ocean acidification in times of ocean warming: a physiologist's view. Mar. Ecol. Prog. Ser. 373, 203-217.
46. 2. Nature 407, 364-367.
47. 2. Science 305, 367-371. (Pubitemid 38938147)
48. Strathmann, M. F. (1987). Reproduction and development of marine invertebrates of the northern Pacific coast: data and methods for the study of eggs, embryos, and larvae. Seattle, WA: University of Washington Press.
49. Strathmann, R. R. (1975). Larval feeding in echinoderms. Am. Zool. 15, 717-730.
50. Strathmann, R. R. and Grünbaum, D. (2006). Good eaters, poor swimmers: compromises in larval form. Integr. Comp. Biol. 46, 312-322. (Pubitemid 44290596)
51. 2-induced seawater acidification impacts sea urchin larval development I: elevated metabolic rates decrease scope for growth and induce developmental delay. Comp. Biochem. Physiol. 160 A, 331-340.
52. 2-driven seawater acidification. J. Exp. Biol. 212, 2579-2594.
53. Underwood, A. J. and Fairweather, P. G. (1989). Supply-side ecology and benthic marine assemblages. Trends Ecol. Evol. 4, 16-20.
54. Widdicombe, S. and Spicer, J. I. (2008). Predicting the impact of ocean acidification on benthic biodiversity: what can animal physiology tell us? J. Exp. Mar. Biol. Ecol. 366, 187-197.
55. Wood, H. L., Spicer, J. I. and Widdicombe, S. (2008). Ocean acidification may increase calcification rates, but at a cost. Proc. R. Soc. Lond. B 275, 1767-1773. (Pubitemid 351839885)
56. 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. Proc. Natl. Acad. Sci. USA 105, 18848-18853.
57. Young, C. M. (1995). Behavior and locomotion during the dispersal phase of larval life. In Ecology of Marine Invertebrate Larvae (ed. L. McEdward), pp. 249-277. Boca Raton, FL: CRC Press.
58. Zar, J. H. (1996). Biostatistical analysis. London: Prentice Hall International (UK) Limited.