Shell condition and survival of puget sound pteropods are impaired by ocean acidification conditions

PLoS ONE

Volumn 9, Issue 8, 2014, Pages

  Busch, D Shallin ^a,b   Maher, Michael ^a   Thibodeaub, Patricia ^a,c   McElhany, Paul ^a  

^a NORTHWEST FISHERIES SCIENCE CENTER   (United States)

^b NATIONAL MARINE FISHERIES SERVICE   (United States)

^c VIRGINIA INSTITUTE OF MARINE SCIENCE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CARBONATE; CARBON DIOXIDE;

ACIDIFICATION; ANIMAL EXPERIMENT; ANIMAL SHELL; ARTICLE; CONTROLLED STUDY; DISSOLUTION; ESTUARY; LIMACINA HELICINA; MARINE SNAIL; MORTALITY; NONHUMAN; OCEAN ACIDIFICATION; OCEAN CURRENT; SEASONAL VARIATION; SEAWATER UPWELLING; STARVATION; SURVIVAL RATE; UNITED STATES; WATER AND WATER RELATED PHENOMENA; ANIMAL; BIOLOGICAL MODEL; GASTROPOD; PACIFIC OCEAN; PH; SEASON;

ANIMAL SHELLS; ANIMALS; GASTROPODA; HYDROGEN-ION CONCENTRATION; MODELS, BIOLOGICAL; PACIFIC OCEAN; SEASONS;

EID: 84940339476     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0105884     Document Type: Article

References (70)

1. Sabine CL, Feely RA, Gruber N, Key RM, Lee K, et al. (2004) The oceanic sink for anthropogenic CO2. Science 305: 367-371.
2. Le Quéré C, Takahashi T, Buitenhuis ET, Rödenbeck C, Sutherland SC (2010) Impact of climate change and variability on the global oceanic sink of CO2. Global Biogeochemical Cycles 24: GB4007.
3. Canadell JG, Le Quéré C, Raupach MR, Field CB, Buitenhuis ET, et al. (2007) Contributions to accelerating atmospheric CO2 growth from economic activity, carbon intensity, and efficiency of natural sinks. Proceedings of the National Academy of Sciences 104: 18866-18870.
4. Orr JC, Fabry VJ, Aumont L, Bopp L, Doney SC, et al. (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437: 681-686. (Pubitemid 41486531)
5. Feely RA, Doney SC, Cooley SR (2009) Ocean acidification: present conditions and future changes in a high-CO2 world. Oceanography 22: 36-47.
6. Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425: 365-365.
7. Solomon S, Qin D, Manning M, Chen Z, Marquis M, et al, editors (2007) Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge and New York.
8. Beardall J, Stojkovic S, Larsen S (2009) Living in a high CO2 world: impacts of global climate change on marine phytoplankton. Plant Ecology & Diversity 2: 191-205.
9. Nilsson GE, Dixson DL, Domenici P, McCormick MI, Sorensen C, et al. (2012) Near-future carbon dioxide levels alter fish behaviour by interfering with neurotransmitter function. Nature Climate Change 2: 201-204.
10. Kroeker KJ, Kordas RL, Crim RN, Singh GG (2010) Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecology Letters 13: 1419-1434.
11. Ainsworth CH, Samhouri JF, Busch DS, Chueng WWL, Dunne J, et al. (2011) Potential impacts of climate change on Northeast Pacific marine fisheries and food webs. ICES Journal of Marine Science 68: 1217-1229.
12. Hall-Spencer JM, Rodolfo-Metalpa R, Martin S, Ransome E, Fine M, et al. (2008) Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454: 96-99. (Pubitemid 351931977)
13. Hönisch B, Ridgwell A, Schmidt DN, Thomas E, Gibbs SJ, et al. (2012) The geological record of ocean acidification. Science 335: 1058-1063.
14. Busch DS, Harvey CJ, McElhany P (2013) Potential impacts of ocean acidifcation on the Puget Sound food web. ICES Journal of Marine Science 70: 823-833.
15. Brodeur RD, Lorz RD, Pearcy WG (1987) Food habits and dietary variability of pelagic nekton off Oregon and Washington, 1979-1984. U.S. Dept. Commerce, NOAA Tech. Memo. NMFS-57. 32 p.
16. Aydin KY, McFarlane GA, King JR, Megrey BA, Myers KW (2005) Linking oceanic food webs to coastal production and growth rates of Pacific salmon (Oncorhynchus spp.), using models on three scales. Deep Sea Research Part II: Topical Studies in Oceanography 52: 757-780. (Pubitemid 40534518)
17. Armstrong JL, Boldt JL, Cross AD, Moss JH, Davis ND, et al. (2005) Distribution, size, and interannual, seasonal and diel food habits of northern Gulf of Alaska juvenile pink salmon, Oncorhynchus gorbuscha. Deep Sea Research Part II: Topical Studies in Oceanography 52: 247-265. (Pubitemid 40323610)
18. Brodeur RD, Daly EA, Sturdevant MV, Miller TW, Moss JH, et al. (2007) Regional comparisons of juvenile salmon (Oncorhynchus spp.) feeding in coastal marine waters off the West Coast of North America. American Fisheries Society Symposium 57: 183-203.
19. Comeau S, Gorsky G, Alliouane S, Gattuso JP (2010) Larvae of the pteropod Cavolina inflexa exposed to aragonite undersaturation are viable but shell-less. Marine Biology Letters 157: 2341-2345.
20. Comeau S, Gorsky G, Jeffree R, Teyssié J-L, Gattuso JP (2009) Impact of ocean acidification on a key Arctic pelagic mollusc (Limacina helicina). Biogeosciences 6: 1877-1882.
21. Comeau S, Jeffree R, Teyssié J-L, Gattuso J-P (2010) Response of the arctic pteropod Limacina helicina to projected future environmental conditions. PLoS ONE 5: e11362.
22. Lischka S, Budenbender J, Boxhammer T, Riebesell U (2011) Impact of ocean acidification and elevated temperatures on early juveniles of the polar shelled pteropod Limacina helicina: mortality, shell degradation, and shell growth. Biogeosciences 8: 919-932.
23. Comeau S, Alliouane S, Gattuso JP (2012) Effects of ocean acidification on overwintering juvenile Arctic pteropods Limacina helicina. Marine Ecology Progress Series 456: 279-284.
24. Lischka S, Riebesell U (2012) Synergistic effects of ocean acidification and warming on overwintering pteropods in the Arctic. Global Change Biology 18: 3417-3528.
25. Bednaršek N, Tarling GA, Bakker DCE, Fielding S, Cohen A, et al. (2012) Description and quantification of pteropod shell dissolution: a sensitive bioindicator of ocean acidification. Global Change Biology 18: 2378-2388.
26. Bednaršek N, Tarling GA, Bakker DCE, Fielding S, Jones EM, et al. (2012) Extensive dissolution of live pteropods in the Southern Ocean. Nature Geosciences 5: 881-885.
27. Mackas DL, Galbraith MD (2012) Pteropod time-series from the NE Pacific. ICES Journal of Marine Science 69: 448-459.
28. Gannefors C, Böer M, Kattner G, Graeve M, Eiane K, et al. (2005) The Arctic sea butterfly Limacina helicina: lipids and life strategy. Marine Biology 147: 169-177. (Pubitemid 40689505)
29. Comeau S, Gattuso JP, Nisumaa AM, Orr J (2012) Impact of aragonite saturation state changes on migratory pteropods. Proceedings of the Royal Society B-Biological Sciences 279: 732-738.
30. Sato-Okoshi W, Okoshi K, Sasaki H, Akiha F (2010) Shell structure characteristics of pelagic and benthic molluscs from Antarctic waters. Polar Science 4: 257-261.
31. Collier R, Dymond J, Honjo S, Manganini S, Francois R, et al. (2000) The vertical flux of biogenic and lithogenic material in the Ross Sea: moored sediment trap observations 1996-1998. Deep Sea Research Part II: Topical Studies in Oceanography 47: 3491-3520. (Pubitemid 32039895)
32. Honjo S (2004) Particle export and the biological pump in the Southern Ocean. Antarctic Science 16: 501-516.
33. Feely RA, Sabine CL, Lee K, Berelson W, Kleypas J, et al. (2004) Impact of anthropogenic CO2 on the CaCO3 system in the oceans. Science 305: 362-366.
34. Feely RA, Sabine CL, Hernandez-Ayon JM, Ianson D, Hales B (2008) Evidence for upwelling of corrosive "acidified" water onto the continental shelf. Science 320: 1490-1492. (Pubitemid 351929427)
35. Hauri C, Gruber N, Plattner G-K, Alin S, Feely RA, et al. (2009) Ocean acidification in the California current system. Oceanography 22: 61-71.
36. Feely RA, Sabine CL, Byrne RH, Millero FJ, Dickson AG, et al. (2012) Decadal changes in the aragonite and calcite saturation state of the Pacific Ocean. Global Biogeochem Cycles 26: GB3001.
37. Bakun A (1990) Global climate change and intensification of coastal ocean upwelling. Science 247: 198-201.
38. Rykaczewski RR, Checkley DM (2008) Influence of ocean winds on the pelagic ecosystem in upwelling regions. Proceedings of the National Academy of Sciences 105: 1965-1970. (Pubitemid 351439448)
39. Gruber N, Hauri C, Lachkar Z, Loher D, Frölicher TL, et al. (2012) Rapid progression of ocean acidification in the California Current System. Science 337: 220-223.
40. Feely RA, Alin SR, Newton J, Sabine CL, Warner M, 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.
41. Reum JCP, Alin SR, Feely RA, Newton J, Warner M, et al. (2014) Seasonal carbonate chemistry covariation with temperature, oxygen, and salinity in a fjord estuary: implications for the design of ocean acidification experiments. PLoS ONE 9: e89619.
42. Rosenthal JJC, Seibel BA, Dymowska A, Bezanilla F (2009) Trade-off between aerobic capacity and locomotor capability in an Antarctic pteropod. Proceedings of the National Academy of Sciences 106: 6192-6196.
43. Parker LM, Ross PM, O'Connor WA, Borysko L, Raftos DA, et al. (2012) Adult exposure influences offspring response to ocean acidification in oysters. Global Change Biology 18: 82-92.
44. Sunday JM, Crim RN, Harley CDG, Hart MW (2012) Quantifying rates of evolutionary adaptation in response to ocean acidification. PLoS ONE 6: e22881.
45. Maas AE, Wishner KF, Seibel BA (2012) The metabolic response of pteropods to acidification reflects natural CO2-exposure in oxygen minimum zones. Biogeosciences 9: 747-757.
46. Ohman MD, Lavaniegos BE, Townsend AW (2009) Multi-decadal variations in calcareous holozooplankton in the California Current System: Thecosome pteropods, heteropods, and foraminifera. Geophysical Research Letters 36: L18608.
47. Hunt BPV, Pakhomov EA, Hosie GW, Siegel V, Ward P, et al. (2008) Pteropods in Southern Ocean ecosystems. Progress in Oceanography 78: 193-221.
48. Bathmann UV, Noji TT, von Bodungen B (1991) Sedimentation of pteropods in the Norwegian Sea in autumn. Deep Sea Research Part A Oceanographic Research Papers 38: 1341-1360.
49. Dickson AG, Sabine CL, Christian JR, editors (2007) Guide to best practices for ocean CO2 measurements: PICES Special Publication 3. 191 p.
50. Lewis E, Wallace DWR (2012) Program developed for CO2 system calculations. ORNL/CDIAC-105. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, US Department of Energy, Oak Ridge, Tennessee.
51. Lueker TJ, Dickson AG, Keeling CD (2000) Ocean pCO2 calculated from dissolved inorganic carbon, alkalinity, and equations for K1 and K2: validation based on laboratory measurements of CO2 in gas and seawater at equilibrium. Marine Chemistry 70: 105-119.
52. Dickson AG (1990) Standard potential of the reaction: AgCl (s)+1/2 H2(g)=Ag(s)+HCl(aq), and the standard acidity constant of the ion HSO 4- in synthetic seawater from 273.15 to 318.15 K. Journal of Chemical Thermodynamics 22: 113-124.
53. Uppstrom LR (1974) The boron/chloronity ratio of deep-sea water from the Pacific Ocean. Deep-Sea Research 21: 161-162.
54. R Development Core Team (2013) R: a language and environment for statistical computing, version 2.15.2.
55. Burnham KP, Anderson DR (1998) Model selection and inference: a practical information-theorhetic approach, Second edition. New York: Springer-Verlag. 488 p.
56. van Belle G (2002) Statistical rules of thumb. New York: John Wiley and Sons. 304 p.
57. Bednaršek N, Feely RA, Reum JCP, Peterson B, Menkel J, et al. (2014) Limacina helicina shell dissolution as an indicator of declining habitat suitability due to ocean acidification in the California Current Ecosystem. Proceedings of the Royal Society B: Biological Sciences 281: 20140123.
58. Melzner F, Stange P, Trübenbach K, Thomsen J, Casties I, et al. (2011) Food supply and seawater pCO2 impact calcification and internal shell dissolution in the Blue Mussel Mytilus edulis. PLoS ONE 6: e24223.
59. 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.
60. Hettinger A, Sanford E, Hill TM, Hosfelt JD, Russell AD, et al. (2013) The influence of food supply on the response of Olympia oyster larvae to ocean acidification. Biogeosciences 10: 6629-6638.
61. Seibel BA, Maas AE, Dierssen HM (2012) Energetic plasticity underlies a variable response to ocean acidification in the pteropod, Limacina helicina antarctica. PLoS ONE 7: e30464.
62. Holcomb M, McCorkle DC, Cohen AL (2010) Long-term effects of nutrient and CO2 enrichment on the temperate coral Astrangia poculata (Ellis and Solander, 1786). Journal of Experimental Marine Biology and Ecology 386: 27-33.
63. Holcomb M, Cohen A, McCorkle D (2012) An investigation of the calcification response of the scleractinian coral Astrangia poculata to elevated pCO2 and the effects of nutrients, zooxanthellae and gender. Biogeosciences 9: 29-39.
64. Maas A, Elder L, Dierssen H, Seibel B (2011) Metabolic response of Antarctic pteropods (Mollusca: Gastropoda) to food deprivation and regional productivity. Marine Ecology Progress Series 441: 129-139.
65. Seibel BA, Dierssen HM (2003) Cascading trophic impacts of reduced biomass in the Ross Sea, Antarctica: just the tip of the iceberg? The Biological Bulletin 205: 93-97. (Pubitemid 37358536)
66. Parker L, Ross P, Connor W, Pörtner H, Scanes E, et al. (2013) Predicting the response of molluscs to the impact of ocean acidification. Biology 2: 651-692.
67. Cannon CA (1983) An overview of circulation in the Puget Sound estuarine system. U.S. Dept. Commerce, NOAA Tech. Memo. ERL PMEL-48. 30 p.
68. Snover AK, Mote PW, Whitely Binder L, Hamlet AF, Mantua NJ (2005) Uncertain future: climate change and its effects on Puget Sound. A report for the Puget Sound Action Team by the Climate Impacts Group (Center for Science in the Earth System, Joint Institute for the Study of the Atmosphere and Oceans, University of Washington, Seattle). 37 p.
69. Manno C, Morata N, Primicerio R (2012) Limacina retroversa's response to combined effects of ocean acidification and sea water freshening. Estuarine, Coastal and Shelf Science 113: 163-171.
70. Pespeni MH, Sanford E, Gaylord B, Hill TM, Hosfelt JD, et al. (2013) Evolutionary change during experimental ocean acidification. Proceedings of the National Academy of Sciences 110: 6937-6943.