Multigenerational exposure to ocean acidification during food limitation reveals consequences for copepod scope for growth and vital rates

Environmental Science and Technology

Volumn 48, Issue 20, 2014, Pages 12275-12284

  Pedersen, Sindre A ^a   Håkedal, Ole Jacob ^a   Salaberria, Iurgi ^a   Tagliati, Alice ^a,b   Gustavson, Liv Marie ^a   Jenssen, Bjørn Munro ^a   Olsen, Anders J ^a   Altin, Dag ^c  

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^b UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^c BioTrix   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

ACIDIFICATION; ADAPTIVE RADIATION; CARBON DIOXIDE; CRUSTACEAN; FOOD WEB; GROWTH RESPONSE; MARINE ECOSYSTEM; ONTOGENY; POLLUTION EXPOSURE; TROPHIC LEVEL;

ACCLIMATIZATION; ACIDIFICATION; ALGAL GROWTH; ARTICLE; BODY GROWTH; CALANUS FINMARCHICUS; CONTROLLED STUDY; COPEPOD; DRY WEIGHT; EGG PRODUCTION; ENERGY EXPENDITURE; FEMALE; FERTILITY; FOOD AVAILABILITY; GAS MIXING; HATCHING; NONHUMAN; OCEAN ACIDIFICATION; ONTOGENY; SEA POLLUTION; ANIMAL; CHEMISTRY; EATING; ECOSYSTEM; FOOD CHAIN; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PH; PHYTOPLANKTON; SEA;

ATLANTIC OCEAN; ATLANTIC OCEAN (NORTH);

COPEPODA;

CARBON DIOXIDE; SEA WATER;

ANIMALS; CARBON DIOXIDE; COPEPODA; EATING; ECOSYSTEM; FOOD CHAIN; HYDROGEN-ION CONCENTRATION; OCEANS AND SEAS; PHYTOPLANKTON; SEAWATER;

EID: 84908139508     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es501581j     Document Type: Article

References (74)

1. Solomon, S. Intergovernmental Panel on Climate Change.; Intergovernmental Panel on Climate Change. Working Group I. Climate change 2007: The physical science basis: contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press: Cambridge; New York, 2007; p viii.
2. Houghton, J. T. Intergovernmental Panel on Climate Change. Working Group I. Climate change 2001: The scientific basis: contribution of Working Group I to the third assessment report of the Intergovernmental Panel on Climate Change; Cambridge University Press: Cambridge; New York, 2001; p 881.
3. Caldeira, K.; Wickett, M. E. Anthropogenic carbon and ocean pH Nature 2003, 425 (6956) 365-365
4. Raven, J.; Caldeira, K.; Elderfield, H.; Hoegh-Guldberg, O.; Liss, P.; Riebesell, U.; Shepherd, J.; Turley, C.; Watson, A. Ocean acidification due to increasing atmospheric carbon dioxide; Royal Society: London, 2005; p 60.
5. Harvey, B. P.; Gwynn-Jones, D.; Moore, P. J. Meta-analysis reveals complex marine biological responses to the interactive effects of ocean acidification and warming Ecol. Evolution 2013, 3 (4) 1016-1030
6. 2 tolerance in marine ectothermic animals: pre-adaptation through lifestyle and ontogeny? Biogeosciences 2009, 6 (10) 2313-2331
7. Fitzer, S. C.; Caldwell, G. S.; Close, A. J.; Clare, A. S.; Upstill-Goddard, R. C.; Bentley, M. G. Ocean acidification induces multi-generational decline in copepod naupliar production with possible conflict for reproductive resource allocation Journal of Experimental Marine Biology and Ecology 2012, 418, 30-36
8. 2 affects embryonic development and larval phototaxis in a temperate marine fish Ecol. Evolution 2013, 3 (11) 3637-3646
9. Munday, P. L.; Dixson, D. L.; McCormick, M. I.; Meekan, M.; Ferrari, M. C. O.; Chivers, D. P. Replenishment of fish populations is threatened by ocean acidification Proc. Natl. Acad. Sci. U.S.A. 2010, 107 (29) 12930-12934
10. Planque, B.; Batten, S. D. Calanus finmarchicus in the North Atlantic: the year of Calanus in the context of interdecadal change Ices Journal of Marine Science 2000, 57 (6) 1528-1535
11. Conover, R. J. Comparative life histories in the genera Calanus and Neocalanus in high-latitudes of the northern hemisphere Hydrobiologia 1988, 167, 127-142
12. Campbell, R. G.; Wagner, M. M.; Teegarden, G. J.; Boudreau, C. A.; Durbin, E. G. Growth and development rates of the copepod Calanus finmarchicus reared in the laboratory Mar. Ecol.: Prog. Ser. 2001, 221, 161-183
13. Runge, J. A. Should we expect a relationship between primary production and fisheries-the role of copepod dynamics as a filter of trophic variability Hydrobiologia 1988, 167, 61-71
14. Beaugrand, G.; Kirby, R. R. Climate, plankton and cod Global Change Biology 2010, 16 (4) 1268-1280
15. Kwasniewski, S.; Gluchowska, M.; Walkusz, W.; Karnovsky, N. J.; Jakubas, D.; Wojczulanis-Jakubas, K.; Harding, A. M. A.; Goszczko, I.; Cisek, M.; Beszczynska-M?ller, A.; Walczowski, W.; Weslawski, J. M.; Stempniewicz, L. Interannual changes in zooplankton on the West Spitsbergen Shelf in relation to hydrography and their consequences for the diet of planktivorous seabirds Ices Journal of Marine Science 2012, 69 (5) 890-901
16. Bathmann, U. V.; Noji, T. T.; Voss, M.; Peinert, R. Copepod fecal pellets-abundance, sedimentation and content at a permanent station in the Norwegian Sea in May June 1986 Mar. Ecol.: Prog. Ser. 1987, 38 (1) 45-51
17. 2-induced acidification affects hatching success in Calanus finmarchicus Mar. Ecol.: Prog. Ser. 2007, 350, 91-97
18. Mayor, D. J.; Everett, N. R.; Cook, K. B. End of century ocean warming and acidification effects on reproductive success in a temperate marine copepod J. Plankton Res. 2012, 34 (3) 258-262
19. 2-induced acidification on the reproduction of a key Arctic copepod Calanus glacialis Journal of Experimental Marine Biology and Ecology 2012, 428, 39-42
20. 2-driven seawater acidification on survival, egg production rate and hatching success of four marine copepods Acta Oceanol Sin 2011, 30 (6) 86-94
21. 2 gradients experienced by Arctic copepods under winter sea ice Proc. Natl. Acad. Sci. U.S.A. 2013, 110 (51) E4960-E4967
22. 2-acidified seawater: effects on survival and development Biogeosciences 2013, 10 (11) 7481-7491
23. 2 and temperature on the Arctic calanoid copepods Calanus glacialis and C. hyperboreus Marine Pollution Bulletin 2014, 80 (1-2) 59-70
24. Marshall, D. J. Transgenerational plasticity in the sea: Context-dependent maternal effects across the life history Ecology 2008, 89 (2) 418-427
25. Dupont, S.; Thorndyke, M. C. Ocean acidification and its impact on the early life-history stages of marine animals. In Impacts of Acidification on Biological, Chemical, and Physical Systems in the Mediterranean and Black Seas; Briand, F., Ed.; CIESM Monographs: Monaco, 2008; pp 89-97.
26. Dupont, S.; Dorey, N.; Stumpp, M.; Melzner, F.; Thorndyke, M. Long-term and trans-life-cycle effects of exposure to ocean acidification in the green sea urchin Strongylocentrotus droebachiensis Marine Biology 2013, 160 (8) 1835-1843
27. Pespeni, M. H.; Sanford, E.; Gaylord, B.; Hill, T. M.; Hosfelt, J. D.; Jaris, H. K.; LaVigne, M.; Lenz, E. A.; Russell, A. D.; Young, M. K.; Palumbi, S. R. Evolutionary change during experimental ocean acidification Proc. Natl. Acad. Sci. U.S.A. 2013, 110 (17) 6937-6942
28. 2 seawater on the copepod (Acartia tsuensis) through all life stages and subsequent generations Marine Pollution Bulletin 2008, 56 (6) 1086-1090
29. Cox, P. M.; Betts, R. A.; Jones, C. D.; Spall, S. A.; Totterdell, I. J. Acceleration of global warming due to carbon-cycle feedbacks in a coupled climate model Nature 2000, 408 (6809) 184-187
30. Groger, M.; Maier-Reimer, E.; Mikolajewicz, U.; Moll, A.; Sein, D. NW European shelf under climate warming: implications for open ocean-shelf exchange, primary production, and carbon absorption Biogeosciences 2013, 10 (6) 3767-3792
31. 2 measurements, PICES Special Publication: 2007; Vol. 3, p 191.
32. Tao, X. W.; Ni, Y. Y.; Pu, X. Q.; Yang, C.; Hu, A. P.; Pu, X. Q. Determination of total alkalinity and calcium concentration of seawater rapidly and automaticly with small-amount samples. Third International Conference on Bioinformatics and Biomedical Engineering, Beijing, June 11-13, 2009; Vols. 1-11, pp 5755-5758.
33. 2 system calculations; Carbon Dioxide Information Analysis Center: 1998.
34. Mehrbach, C.; Culberso, Ch; Hawley, J. E.; Pytkowic, Rm Measurement of apparent dissociation-constants of carbonic-acid in seawater at atmospheric-pressure Limnol. Oceanography 1973, 18 (6) 897-907
35. Dickson, A. G.; Millero, F. J. A comparison of the equilibrium-constants for the dissociation of carbonic-acid in seawater media Deep-Sea Res. 1987, 34 (10) 1733-1743
36. Båmstedt, U.; Nejstgaard, J. C.; Solberg, P. T. Utilisation of small-sized food algae by Calanus finmarchicus (Copepoda, Calanoida) and the significance of feeding history Sarsia 1999, 84 (1) 19-38
37. Marshall, S. M.; Orr, A. P. The biology of a marine copepod; Springer-Verlag: Berlin, New York, 1972; p vii.
38. Mauchline, J. The biology of calanoid copepods; Academic Press: San Diego, 1998; p vii.
39. Landry, M. R. The development of marine calanoid copepods with comment on the isochronal rule Limnol. Oceanography 1983, 28 (4) 614-624
40. Hu, Q.; Petrik, C. M.; Davis, C. S. Normal versus gamma: stochastic models of copepod molting rate J. Plankton Res. 2007, 29 (11) 985-997
41. Frost, B. W. Effects of size and concentration of food particles on feeding behavior of marine planktonic copepod Calanus pacificus Limnol. Oceanography 1972, 17 (6) 805-815
42. Miller, C. B.; Morgan, C. A.; Prahl, F. G.; Sparrow, M. A. Storage lipids of the copepod Calanus finmarchicus from Georges Bank and the Gulf of Maine Limnol. Oceanography 1998, 43 (3) 488-497
43. Williams, R.; Robins, D. B. Effects of preservation on wet weight, dry-weight, nitrogen and carbon contents of Calanus helgolandicus (Crustacea, Copepoda) Marine Biology 1982, 71 (3) 271-281
44. Tande, K. S.; Slagstad, D. Assimilation efficiency in herbivorous aquatic organisms-the potential of the ratio method using C-14 and biogenic silica as markers Limnol. Oceanography 1985, 30 (5) 1093-1099
45. Kiorboe, T.; Mohlenberg, F.; Hamburger, K. Bioenergetics of the planktonic copepod Acartia tonsa-Relation between feeding, egg-production and respiration, and composition of specific dynamic action Mar. Ecol.: Prog. Ser. 1985, 26 (1-2) 85-97
46. Gnaiger, E. Calculation of energetic and biochemical equivalents of respiratory oxygen consumption. In Polarographic oxygen sensors: aquatic and physiological applications; Gnaiger, E.; Forstner, H., Eds.; Springer-Verlag: Berlin, New York, 1983.
47. Widdows, J.; Johnson, D. Physiological Energetics of Mytilus edulis-Scope for Growth Mar. Ecol.: Prog. Ser. 1988, 46 (1-3) 113-121
48. Little, R. J. A. A test of missing completely at random for multivariate data with missing values J. Am. Stat. Assoc. 1988, 83 (404) 1198-1202
49. 2 impact calcification and internal shell dissolution in the blue mussel Mytilus edulis PloS one 2011, 6 (9 e24223 10.1371/journal.pone.0024223
50. Thomsen, J.; Casties, I.; Pansch, C.; Kortzinger, A.; Melzner, F. Food availability outweighs ocean acidification effects in juvenile Mytilus edulis: laboratory and field experiments Global change biology 2013, 19 (4) 1017-1027
51. 2 induced seawater acidification Aquatic toxicology 2012, 110, 194-207
52. Beniash, E.; Ivanina, A.; Lieb, N. S.; Kurochkin, I.; Sokolova, I. M. Elevated level of carbon dioxide affects metabolism and shell formation in oysters Crassostrea virginica Mar. Ecol.: Prog. Ser. 2010, 419, 95-108
53. Thomsen, J.; Melzner, F. Moderate seawater acidification does not elicit long-term metabolic depression in the blue mussel Mytilus edulis Marine Biology 2010, 157 (12) 2667-2676
54. 2 ocean Marine pollution bulletin 2012, 64 (4) 699-703
55. 2 induced seawater acidification impacts sea urchin larval development I: Elevated metabolic rates decrease scope for growth and induce developmental delay Comp. Biochem. Phys. A 2011, 160 (3) 331-340
56. Deigweiher, K.; Hirse, T.; Bock, C.; Lucassen, M.; Portner, H. O. Hypercapnia induced shifts in gill energy budgets of Antarctic notothenioids J. Comp. Physiol. B 2010, 180 (3) 347-359
57. Place, S. P.; Smith, B. W. Effects of seawater acidification on cell cycle control mechanisms in Strongylocentrotus purpuratus embryos PloS one 2012, 7 (3 e34068 10.1371/journal.pone.0034068
58. 2 additively regulate physiology, morphology and genomic responses of larval sea urchins, Strongylocentrotus purpuratus Proc. R. Soc. B-Biol. Sci. 2013, 280 (1759 20130155 10.1098/rspb.2013.0155
59. Dorey, N.; Lancon, P.; Thorndyke, M.; Dupont, S. Assessing physiological tipping point of sea urchin larvae exposed to a broad range of pH Global change biology 2013, 19 (11) 3355-3367
60. Dupont, S.; Lundve, B.; Thorndyke, M. Near future ocean acidification increases growth rate of the lecithotrophic larvae and juveniles of the sea star Crossaster papposus J. Exp. Zool. Part B 2010, 314B (5) 382-389
61. Dupont, S.; Thorndyke, M. C. Direct impacts of near-future ocean acidification on sea urchins. In Climate Change Perspectives From the Atlantic: Past, Present and Future; Fernández-Palacios, J. M.; de Nascimiento, L.; Hernández, J. C.; Clemente, S.; González, A.; Díaz-González, J. P., Eds.; Servicio de Publicaciones de La Universidad de La Laguna: La Laguna, Spain, 2013; pp 461-485.
62. 2-driven acidification Marine environmental research 2014, 93, 70-77
63. Richardson, K.; Jónasdóttir, S.; Hay, S. J.; Christoffersen, A. Calanus finmarchicus egg production and food availability in the Faroe-Shetland Channel and northern North Sea: October-March Fish. Oceanogr. 1999, 8 (Suppl. 1) 153-162
64. Diel, S.; Tande, K. Does the spawning of Calanus finmarchicus in high-latitudes follow a reproducible pattern Marine Biology 1992, 113 (1) 21-31
65. Nielsen, T. G.; Hansen, B. Plankton community structure and carbon cycling on the western coast of greenland during and after the sedimentation of a diatom bloom Mar. Ecol.: Prog. Ser. 1995, 125 (1-3) 239-257
66. Vehmaa, A.; Brutemark, A.; Engstrom-Ost, J. Maternal effects may act as an adaptation mechanism for copepods facing pH and temperature changes PloS one 2012, 7 (10 e48538 10.1371/journal.pone.0048538
67. 2 conditions on the survival and growth of the marine shrimp Palaemon pacificus Journal of Experimental Marine Biology and Ecology 2008, 367 (1) 41-46
68. 2 concentration on the egg production rate and early development of two marine copepods (Acartia steueri and Acartia erythraea) Marine pollution bulletin 2004, 49 (9-10) 721-727
69. 2 on the reproduction of two calanoid copepods Marine pollution bulletin 2013, 73 (2) 428-434
70. 2) concentrations on early developmental stages of the marine copepod Calanus finmarchicus Gunnerus (Copepoda: Calanoidae) Journal of Toxicology and Environmental Health, Part A 2014, 77, 535-549
71. McDonald, M. R.; McClintock, J. B.; Amsler, C. D.; Rittschof, D.; Angus, R. A.; Orihuela, B.; Lutostanski, K. Effects of ocean acidification over the life history of the barnacle Amphibalanus amphitrite Mar. Ecol.: Prog. Ser. 2009, 385, 179-187
72. Dupont, S.; Ortega-Martinez, O.; Thorndyke, M. Impact of near-future ocean acidification on echinoderms Ecotoxicology 2010, 19 (3) 449-462
73. 2 and the effect of parent acclimation on development in the tropical Pacific sea urchin Echinometra mathaei Marine Biology 2013, 160 (8) 1913-1926
74. Byrne, M.; Prowse, T. A. A.; Sewell, M. A.; Dworjanyn, S.; Williamson, J. E.; Vaitilingon, D. Maternal provisioning for larvae and larval provisioning for juveniles in the toxopneustid sea urchin Tripneustes gratilla Marine Biology 2008, 155 (5) 473-482