Response of Copepods to Elevated pCO2 and Environmental Copper as Co-Stressors - A Multigenerational Study

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Fitzer, Susan C ^a,b   Caldwell, Gary S ^a   Clare, Anthony S ^a   Upstill Goddard, Robert C ^a   Bentley, Matthew G ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; COPPER; PHOSPHORUS; SULFUR;

ACIDIFICATION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOCHEMICAL COMPOSITION; BLOOD CARBON DIOXIDE TENSION; BODY GROWTH; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; COPEPOD; ENVIRONMENTAL FACTOR; ENVIRONMENTAL IMPACT ASSESSMENT; ENVIRONMENTAL STRESS; FEMALE; NONHUMAN; PH MEASUREMENT; TISBE BATTAGLIAI;

ANIMALS; CARBON DIOXIDE; COPEPODA; COPPER; ECOSYSTEM; FEMALE; FERTILITY; HYDROGEN-ION CONCENTRATION; OCEANS AND SEAS; SEAWATER; SPECTROPHOTOMETRY, ATOMIC; TIME FACTORS; WATER POLLUTANTS, CHEMICAL;

EID: 84881341619     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0071257     Document Type: Article

References (81)

1. Gibbs SJ, Stoll HM, Brown PR, Bralower TJ, (2010) Ocean acidification and surface water carbonate production across the Paleocene-Eocene thermal maximum. Earth Planet Sci Lett 295: 583-592.
2. Clapham ME, Payne JL, (2011) Acidification, anoxia, and extinction: A multiple logistic regression analysis of extinction selectivity during the Middle and Late Permian. Geology 39: 1059-1062.
3. Ogden DE, Sleep NH, (2012) Explosive eruption of coal and basalt and the end-Permian mass extinction. Proc Nat Acad Sci USA 109: 59-62.
4. Doney SC, Fabry VJ, Feely RA, Kleypas JA, (2009) Ocean acidification: The other CO2 problem. Ann Rev Mar Sci 1: 169-192.
5. IPCC (2007) Climate Change 2007: the fourth assessment report of the Intergovernmental Panel on Climate Change (IPCC). Cambridge University Press, Cambridge, UK.
6. Ferrari MCO, McCormick MI, Munday PL, Meekan MG, Dixson DL, et al. (2011) Putting prey and predator into the CO2 equation- qualitative and quantitative effects of ocean acidifation on predator-prey interactions. Ecology Letters 14: 1143-1148.
7. 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.
8. Mathis JT, Cross JN, Bates NR, (2011) The role of ocean acidification in systemic carbonate mineral suppression in the Bering Sea. Geophys Res Lett 38: L19602.
9. Tyrell T, (2011) Anthropogenic modification of the oceans. Philos Trans R Soc A 369: 887-908.
10. Caldeira K, Wickett ME, (2003) Anthropogenic carbon and ocean pH. Nature 425: 365.
11. Anthony KRN, Maynard JA, Diaz-Pulido G, Mumby PJ, Marshall PA, et al. (2011a) Ocean acidification and warming will lower coral reef resilience. Glob Chang Biol 17: 1798-1808.
12. Cooley SR, Kite-Powell HL, Doney SC, (2009) Ocean acidification's potential to alter global ecosystem services. Oceanography 22: 172-181.
13. Meakin NG, Wyman M, (2011) Rapid shifts in picoeukaryote community structure in response to ocean acidification. ISME Journal 5: 1397-1405.
14. Byrne M, (2012) Global change ecotoxicology: Identification of early life history bottlenecks in marine invertebrates, variable species responses and variable experimental approaches. Mar Environ Res 76: 3-15.
15. Dupont S, Thorndyke MC, (2009) Impact of CO2-driven ocean acidification on invertebrates early life-hystory-What we know, what we need to know and what we can do. Biogeosci Discuss 6: 3109-3131.
16. Fitzer SC, Caldwell GS, Close AJ, Clare AS, Upstill-Goddard RC, et al. (2012a) Ocean acidification induces multi-generational decline in copepod naupliar production with possible conflict for reproductive resource allocation. J Exp Mar Biol Ecol 418-19: 30-36.
17. Kurihara H, Ishimatsu A, (2008) Effects of high CO2 seawater on the copepod (Acartia tsuensis) through all life stages and subsequent generations. Mar Pollut Bull 56: 1086-1090.
18. Sunday JM, Crim RN, Harley CDG, Hart MW, (2011) Quantifying rates of evolutionary adaptation in response to ocean acidification. PLoS ONE 6: e22881.
19. Denman K, Brasseur G, Chidthaisong A, Ciais P, Cox PM,et al. (2007) Couplings between changes in the climate system and biogeochemistry. In Climate Change 2007: The Physical Science Basis. Contributing of Working Group 1 to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. [Solomon S, Qin D, Manning M, Chen Z, Marquis M Averyt KB, Tignor M and Miller HL (eds.)]. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA.
20. Araujo CVM, Diz FR, Tornero V, Lubian LM, Moreno-Garrido I, (2010) Ranking sediment samples from three Spanish estuaries in relation to its toxicity for two benthic species: The microalga Cylindrotheca closterium and the copepod Tisbe battagliai. Environ Toxicol Chem 29: 393-400.
21. Geffard O, Geffard A, Budzinski H, Crouzet C, Menasria R, et al. (2005) Mobility and potential toxicity of sediment-bound metals in a tidal estuary. Environ Toxicol 20: 407-417.
22. Green AS, Chandler GT, Blood ER, (1993) Aqueous-, pore-water-, and sediment-phase cadmium: Toxicity relationships for a meiobenthic copepod. Environ Toxicol Chem 12: 1497-1506.
23. Hagopian-Schlekat T, Chandler GT, Shaw TJ, (2001) Acute toxicity of five sediment-associated metals, individually and in a mixture, to the estuarine meiobenthic harpacticoid copepod Amphiascus tenuiremis. Mar Environ Res 51: 247-264.
24. Millero FJ, Santana-Casiano JM, González-Dávila M, (2010) The formation of Cu(II) complexes with carbonate and bicarbonate ions in NaClO4 solutions. J Solution Chem 39: 543-558.
25. Richards R, Chaloupka M, Sanò M, Tomlinson R, (2011) Modelling the effects of 'coastal' acidification on copper speciation. Ecol Modell 222: 3559-3567.
26. Barka S, Pavillon J-F, Amiard JC, (2001) Influence of different essential and non-essential metals on MTLP levels in the copepod Tigriopus brevicornis. Comp Biochem Physiol Part C 128: 479-493.
27. Anlauf H, D'Croz L, O'Dea A, (2011) A corrosive concoction: The combined effects of ocean warming and acidification on the early growth of a stony coral are multiplicative. J Exp Mar Biol Ecol 397: 13-20.
28. Anthony KRN, Kleypas JA, Gattuso JP, (2011b) Coral reefs modify their seawater carbon chemistry- implications for impacts of ocean acidification. Glob Chang Biol 17: 3655-3666.
29. Byrne M, Ho M, Selvakumaraswamy P, Nguyen HD, Dworjanyn SA, et al. (2009) Temperature, but not pH, compromises sea urchin fertilization and early development under near-future climate change scenarios. Proc R Soc Lond B Biol Sci 276: 1883-1888.
30. Byrne M, Soars N, Selvakumaraswamy P, Dworjanyn SA, Davis AR, (2010) Sea urchin fertilization in a warm, acidified and high pCO2 ocean across a range of sperm densities. Mar Environ Res 69: 234-239.
31. Egilsdottir H, Spicer JI, Rundle SD, (2009) The effect of CO2 acidified sea water and reduced salinity on aspects of the embryonic development of the amphipod Echinogammarus marinus (Leach). Mar Pollut Bull 58: 1187-1191.
32. Findlay HS, Kendall MA, Spicer JI, Widdicombe S, (2010) Relative influences of ocean acidification and temperature on intertidal barnacle post-larvae at the northern edge of their geographical distribution. Estuar Coast Shelf Sci 86: 675-682.
33. Lacoue-Labarthe T, Martin S, Oberhansli F, Teyssie J-L, Markich S, et al. (2009) Effects of increased pCO2 and temperature on trace element (Ag, Cd and Zn) bioaccumulation in the eggs of the common cuttlefish, Sepia officinalis. Biogeosciences Discuss 6: 4865.
34. O'Donnell MJ, Hammond LM, Hofmann GE, (2009) Predicted impact of ocean acidification on a marine invertebrate: elevated CO2 alters response to thermal stress in sea urchin larvae. Mar Biol 156: 439-446.
35. Parker LM, Ross PM, O'Connor WA, (2009) The effect of ocean acidification and temperature on the fertilisation and embryonic development of the Sydney rock oyster Saccostrea glomerata (Gould 1850). Glob Chang Biol 15: 2123-2136.
36. Pascal P-Y, Fleeger JW, Galvez F, Carman KR, (2010) The toxicological interaction between ocean acidity and metals in coastal meiobenthic copepods. Mar Pollut Bull 60: 2201-2208.
37. Rodolfo-Metalpa R, Houlbreque F, Tambutte E, Boisson F, Baggini C, et al. (2011) Coral and mollusc resistance to ocean acidification adversely affected by warming. Nat Clim Chang 1: 308-312.
38. Barata C, Baird DJ, Medina M, Albalat A, Soares AMVM, (2002) Determining the ecotoxicological mode of action of toxic chemicals in meiobenthic marine organisms: stage specific short tests with Tisbe battagliai. Mar Ecol Prog Ser 230: 183-194.
39. Diz FR, Araujo CVM, Moreno-Garrido I, Hampel M, Blasco J, (2009) Short-term toxicity tests on the harpacticoid copepod Tisbe battagliai: Lethal and reproductive endpoints. Ecotoxicol Environ Saf 72: 1881-1886.
40. Hutchinson TH, Williams TD, Eales GJ, (1994) Toxicity of cadmium, hexavalent chromium and copper to marine fish larvae (Cyprinodon variegatus) and copepods (Tisbe battagliai). Mar Environ Res 38: 275-290.
41. Taylor RL, Caldwell GS, Bentley MG, (2005) Toxicity of algal-derived aldehydes to two invertebrate species: Do heavy metal pollutants have a synergistic effect? Aquat Toxicol 74: 20-31.
42. Thomas KV, Barnard N, Collins K, Eggleton J, (2003) Toxicity characterisation of sediment porewaters collected from UK estuaries using a Tisbe battagliai bioassay. Chemosphere 53: 1105-1111.
43. Frankignoulle M, Borges AV, (2001) Direct and indirect pCO2 measurements in a wide range of pCO2 and salinity values (the Scheldt estuary). Aquat Geochem 7: 267-273.
44. Riebesell U, Fabry VJ, Hansson L, Gattuso JP (2010) Guide to best practices for ocean acidification research and data reporting. Publications Office of European Union, Luxembourg 1-260.
45. Duchart P, Calvert SE, Price NB, (1973) Distribution of trace metals in the pore waters of shallow water marine sediments. Limnol Oceanogr Methods 18: 605-610.
46. Gao Y, Lesven L, Gillan D, Sabbe K, Billon G, et al. (2009) Geochemical behaviour of trace elements in sub-tidal marine sediments of the Belgian coast. Mar Chem 117: 88-96.
47. Kottelat R, Vignati DAL, Garcia-Bravo A, Dominik J, Ferrari BJD, (2010) Characterisation of trace element geochemistry in continuous flow-through microcosms: A preliminary step to environmentally meaningful ecotoxicological experiments. Chemosphere 81: 1407-1415.
48. Santos-Echeandia J, Prego R, Cobelo-Garcia A, Millward GE, (2009) Porewater geochemistry in Galican Ria (NW Iberian Peninsula): Implications for benthic fluxes of dissolved trace elements (Co, Cu, Ni, Pb, V, Zn). Mar Chem 117: 77-87.
49. Giutierrez MF, Gagneten AM, Paggi JC, (2010) Copper and chromium alter life cycle variables and the equiproportional development of the freshwater copepod Notodiaptomus conifer (SARS). Water Air and Soil Pollut 213: 275-286.
50. Dykstra MJ, Mann PC, Elwell MR, Ching SV, (2002) Suggested standard operating procedures (SOPs) for the preparation of electron microscopy samples for toxicology/pathology studies in a GLP environment. Toxicol Pathol 30: 735-743.
51. Mayor DJ, Matthews C, Cook K, Zuur AF, Hay S, (2007) CO2-induced acidification affects hatching success in Calanus finmarchicus. Mar Ecol Prog Ser 350: 91-97.
52. Pinho GLL, Pedroso MS, Rodrigues SC, de Souza SS, Bianchini A, (2007) Physiological effects of copper in the euryhaline copepod Acartia tonsa: Waterborne versus waterborne plus dietborne exposure. Aquat Toxicol 84: 62-70.
53. Crawley MJ (2007) The R book, London: John Wiley & Sons Ltd. 950 pp.
54. Faraway JJ (2005) Extending the linear model with R: Generalized linear mixed effects and nonparametric regression models: Chapman and Hall/CRC. 312 pp.
55. Millar RB, Anderson MJ, (2004) Remedies for pseudoreplication. Fish Res 70: 397-407.
56. Gelman A, Hill J (2007) Data analysis using regression and multilevel/hierarchical models., New York: Cambridge University Press. 648 pp.
57. Lewis C, Clemow K, Holt WV (2012) Metal contamination increases the sensitivity of larvae but not gametes to ocean acidification in the polychaete Pomatoceros lamarckii (Quatrefages). Mar Biol DOI10.1007/s00227-012-2081-8.
58. Roberts DA, Birchenough SNR, Lewis C, Sanders MB, Bolam T, et al. (2013) Oceanacidification increases the toxicity of contaminated sediments. Glob Chang Biol 19: 340-351.
59. Nikinmaa M, (2013) Climate change and ocean acidification- Interactions with aquatic toxicology. Aquat Toxicol 126: 365-372.
60. Lee K, Raisuddin S, Hwang D, Park H, Dahms H, et al. (2008) Two-generation toxicity study on the copepod model species Tigriopus japonicus. Chemosphere 72: 1359-1365.
61. Verriopoulos G, Moraitou-Apostolopoulou M, (1982) Differentiation of the sensitivity to copper and cadmium in different life stages of a copepod. Mar Pollut Bull 13: 123-125.
62. Fitzer SC, Bishop JDD, Caldwell GS, Clare AS, Upstill-Goddard RC, et al. (2012b) Visualisation of the copepod female reproductive system using confocal laser scanning microscopy and two-photon microscopy. J Crust Biol 32: 685-692.
63. Stump M, Wren J, Melzner F, Thorndyke MC, Dupont ST, (2012) CO2 induced seawater acidification impacts sea urchin larval development I: Elevated. Comp Biochem Physiol Part A 160: 331-340.
64. Matson PG, Yu PC, Sewell MA, Hofmann GE, (2012) Development under elevated pCO2 conditions does not affect lipid utilization and protein content in early life-history stages of the purple sea urchin, Strongylocentrotus purpuratus. Biol Bull 223: 312-327.
65. Lundström E, Björlenius B, Brinkmann M, Hollert H, Persson JO, et al. (2010) Comparison of six sewage effluents treated with different treatment technologies-Population level responses in the harpacticoid copepod Nitocra spinipes. Aquat Toxicol 96: 298-307.
66. Dave G, (1984) Effects of copper on growth, reproduction, survival and haemoglobin in Daphnia magna. Comp Biochem Physiol 78C: 439-443.
67. Luckey TD (1975) Hormology with organic compounds. Environmental Quality and Safety, Supplement 1: 81-118.
68. Stebbing ARD & Pomroy AJ, (1978) A sublethal technique for assessing the effects of contaminants using Hydra littoralis. Water Res 12: 631-635.
69. Stebbing ARD, (1981) Hormesis-Stimulation of colony growth in Campanularia flexuosa (Hydroazoa) by copper, cadmium and other toxicants. Aquat Toxicol 1: 227-238.
70. Winner RW (1976) Toxicity of copper to daphnids in reconstituted and natural waters. U.S. Environmental Protection Agency, Ecological Research Series EPA-600/3-76-051.
71. Van Assche F, van Tilborg W, Waeterschoot H (1997) Environmental risk assessment for essential elements, case study: Zinc. In Langley E, Mangas S eds. Zinc-Report of an International Meeting. National Environmental Health Forum Monographs. Adelaide, Australia, 33-47.
72. Hopkin SP (1989) Ecophysiology of Metals in Terrestrial Invertebrates. Elsevier Applied Science, Barking, UK.
73. Bossuyt BTA, Janssen CR, (2004) Influence of multigeneration acclimation to copper on tolerance, energy reserves, and homeostasis of Daphnia magna Straus. Environ Toxicol Chem 23: 2029-2037.
74. Schlegel P, Havenhand JN, Gillings MR, Williamson JE, (2012) Individual variability in reproductive success determines winners and losers under ocean acidification: A case study with sea urchins. PLoS ONE 7: e53118.
75. Rossoll D, Bermúdez R, Hauss H, Schultz KG, Riebesell U, et al. (2012) Ocean acidification-induced food quality deterioration constrains trophic transfer. PLoS ONE 7: e34737.
76. Harish V, Sreepada RA, Suryavanshia U, Shanmuganathanb P, Sumathy A, (2011) Assessing the effect of leachate of copper slag from the ISASMELT process on cell growth and proximate components in microalgae, Chlorella vulgaris (Beijerinck). Toxicol Environ Chem 93: 1399-1412.
77. Van den Berg CMG, Wong PTS, Chau YK, (1979) Measurement of complexing materials excreted from algae and their ability to ameliorate copper toxicity. Journal of the Fish Res Board Can 36: 901-905.
78. Rainbow PS, (1997) Trace metal accumulation in marine invertebrates: Marine biology or marine chemistry? J Mar Biol Assoc U. K. 77: 195-210.
79. Viarengo A, Nott JA, (1993) Mechanisms of heavy metal cation homeostasis in marine invertebrates. Comp Biochem Physiol 104: 355-372.
80. Wang M, Wang G, (2010) Oxidative damage effects in the copepod Tigriopus japonicus Mori experimentally exposed to nickel. Ecotoxicology 19: 273-284.
81. Dam HG, (2013) Evolutionary adaptation of marine zooplankton to global change. Ann Rev Mar Sci 5: 349-370.