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Aquatic Sciences

, Volume 79, Issue 3, pp 733–748 | Cite as

Is the chemical composition of biomass the agent by which ocean acidification influences on zooplankton ecology?

  • Jessica Garzke
  • Ulrich Sommer
  • Stefanie M. H. Ismar
Research Article

Abstract

Climate change impacts prevail on marine pelagic systems and food webs, including zooplankton, the key link between primary producers and fish. Several metabolic, physiological, and ecological responses of zooplankton species and communities to global stressors have recently been tested, with an emerging field in assessing effects of combined climate-related factors. Yet, integrative studies are needed to understand how ocean acidification interacts with global warming, mediating zooplankton body chemistry and ecology. Here, we tested the combined effects of global warming and ocean acidification, predicted for the year 2100, on a community of calanoid copepods, a ubiquitously important mesozooplankton compartment. Warming combined with tested pCO2 increase affected metabolism, altered stable isotope composition and fatty acid contents, and reduced zooplankton fitness, leading to lower copepodite abundances and decreased body sizes, and ultimately reduced survival. These interactive effects of temperature and acidification indicate that metabolism-driven chemical responses may be the underlying correlates of ecological effects observed in zooplankton communities, and highlight the importance of testing combined stressors with a regression approach when identifying possible effects on higher trophic levels.

Keywords

Climate change Acartia sp Body size Fatty acids Fitness Stable isotopes 

Notes

Acknowledgements

The authors thank the BMBF (German Ministry of Education and Research) for funding the project BIOACID II. We especially thank A. Paul, C. Paul, H. Horn, M. Rathmer, D. Riemann, M. Rönspies and L. Gobelius for assistance in the installation of the mesocosm facility, sampling and sample preparation. T. Hansen is thanked for great technical support. A. Ludwig is acknowledged for analyzing DIC and Ashlie Maack for language editing. We thank Stuart Findlay and three anonymous referees for helpful review of our work.

Supplementary material

27_2017_532_MOESM1_ESM.docx (488 kb)
Supplementary material 1 (DOCX 488 KB)

References

  1. Aksnes DL, Ohman MD (1996) A vertical life table approach to zooplankton mortality estimation. Limnol Oceanogr 41:1461–1469. doi: 10.4319/lo.1996.41.7.1461 CrossRefGoogle Scholar
  2. Anderson TR, Hessen DO, Elser JJ, Urabe J (2005) Metabolic stoichiometry and the fate of excess carbon and nutrients in consumers. Am Nat 165:1–15. doi: 10.1086/426598 CrossRefPubMedGoogle Scholar
  3. Bellerby RGJ, Schulz KG, Riebesell U et al (2008) Marine ecosystem community carbon and nutrient uptake stoichiometry under varying ocean acidification during the PeECE III experiment. Biogeosciences 5:1517–1527CrossRefGoogle Scholar
  4. Bi R, Ismar S, Sommer U, Zhao M (2016) Environmental dependence of the correlations between stoichiometric and fatty acid-based indicators of phytoplankton nutritional quality. Limnol Oceanogr 62:334–347. doi: 10.1002/lno.10429 CrossRefGoogle Scholar
  5. Boersma M (2000) The nutritional quality of P-limited algae for Daphnia. Limnol Oceanogr 45:1157–1161CrossRefGoogle Scholar
  6. Boersma M, Mathew KA, Niehoff B et al (2016) Temperature driven changes in the diet preference of omnivorous copepods: no more meat when it's hot? Ecol Lett 19:45–53. doi: 10.1111/ele.12541 CrossRefPubMedGoogle Scholar
  7. Bolker BM, Brooks ME, Clark CJ et al (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135. doi: 10.1016/j.tree.2008.10.008 CrossRefPubMedGoogle Scholar
  8. Boyce DG, Lewis MR, Worm B (2010) Global phytoplankton decline over the past century. Nature 466:591–596. doi: 10.1038/nature09268 CrossRefPubMedGoogle Scholar
  9. Brett MT, Müller-Navarra DC (1997) The role of highly unsaturated fatty acids in aquatic foodweb processes. Freshwater Biol 38:483–499CrossRefGoogle Scholar
  10. Brock TD (1981) Calculating solar-radiation for ecological-studies. Ecol Model 14:1–19. doi: 10.1016/0304-3800(81)90011-9 CrossRefGoogle Scholar
  11. Brown JH, Gillooly JF, Allen AP et al (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789CrossRefGoogle Scholar
  12. Byrne M, Przeslawski R (2013) Multistressor impacts of warming and acidification of the ocean on marine invertebrates’ life histories. Integr Comp Biol 53:582–596. doi: 10.1093/icb/ict049 CrossRefPubMedGoogle Scholar
  13. Cohen J (1992) Statistical power analysis. Curr Dir Psychol Sci 1(3):98–101CrossRefGoogle Scholar
  14. Cottingham KL, Lennon JT, Brown BL (2005) Knowing when to draw the line: designing more informative ecological experiments. Front Ecol Environ 3:145–152. doi: 10.1890/1540-9295(2005)003[0145:KWTDTL]2.0.CO;2 CrossRefGoogle Scholar
  15. Crain CM, Kroeker K, Halpern BS (2008) Interactive and cumulative effects of multiple human stressors in marine systems. Ecol Lett 11:1304–1315. doi: 10.1111/j.1461-0248.2008.01253.x CrossRefPubMedGoogle Scholar
  16. Cripps G, Lindeque P, Flynn K (2014) Parental exposure to elevated pCO2 influences the reproductive success of copepods. J Plankton Res 36:1165–1174. doi: 10.1093/plankt/fbu052 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Cripps G, Flynn KJ, Lindeque PK (2016) Ocean acidification affects the phyto-zoo plankton trophic transfer efficiency. PLoS ONE 11(4):e0151739. doi: 10.1371/journal.pone.0151739 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Darchambeau F, Faerovig PJ, Hessen DO (2003) How Daphnia copes with excess carbon in its food. Oecologia 136:336–346. doi: 10.1007/s00442-003-1283-7 CrossRefPubMedGoogle Scholar
  19. Daufresne M, Lengfellner K, Sommer U (2009) Global warming benefits the small in aquatic ecosystems. PNAS 106:12788–12793. doi: 10.1073/pnas.0902080106 CrossRefPubMedPubMedCentralGoogle Scholar
  20. De Wit P, Dupont S, Thor P (2015) Selection on oxidative phosphorylation and ribosomal structure as a multigenerational response to ocean acidification in the common copepod Pseudocalanus acuspes. Evol Appl. doi: 10.1111/eva.12335 PubMedPubMedCentralGoogle Scholar
  21. Dell AI, Pawar S, Savage VM (2011) Systematic variation in the temperature dependence of physiological and ecological traits. PNAS 108:10591–10596. doi: 10.1073/pnas.1015178108 CrossRefPubMedPubMedCentralGoogle Scholar
  22. DeMott WR, Tessier AJ (2002) Stoichiometric constraints vs. algal defenses: testing mechanisms of zooplankton food limitations. Ecology 83:3426–3433CrossRefGoogle Scholar
  23. Doney SC, Ruckelshaus M, Duffy JE et al (2012) Climate change impacts on marine ecosystems. In: Carlson CA, Giovannoni SJ (eds) Annual review of marine science, vol 4. Annual Reviews, Palo Alto, pp 11–37Google Scholar
  24. Dupont S, Thorndyke MC (2009) Impact of CO2-driven ocean acidification on invertebrates early life-history—what we know, what we need to know and what we can do. Biogeosciences 6:3109–3131CrossRefGoogle Scholar
  25. Edwards M, Richardson AJ (2004) Impact of climate change on marine pelagic phenology and trophic mismatch. Nature 430:881–884CrossRefPubMedGoogle Scholar
  26. Eiane K, Ohman MD (2004) Stage-specific mortality of Calanus finmarchicus, Pseudocalanus elongatus and Oithona similis on Fladen Ground, North Sea, during a spring bloom. Mar Ecol Prog Ser 268:183–193CrossRefGoogle Scholar
  27. Evjemo JO, Tokle N, Vadstein O, Olsen Y (2008) Effect of essential dietary fatty acids on egg production and hatching success of the marine copepod Temora longicornis. J Exp Mar Biol Ecol 365:31–37. doi: 10.1016/j.jembe.2008.07.032 CrossRefGoogle Scholar
  28. Fabry VJ, Seibel BA, Feely RA, Orr JC (2008) Impacts of ocean acidification on marine fauna and ecosystem processes. ICES J Mar Sci 65:414–432. doi: 10.1093/icesjms/fsn048 CrossRefGoogle Scholar
  29. Filstrup CT, Hillebrand H, Heathcote AJ et al (2014) Cyanobacteria dominance influences resource use efficiency and community turnover in phytoplankton and zooplankton communities. Ecol Lett 17:464–474. doi: 10.1111/ele.12246 CrossRefPubMedGoogle Scholar
  30. Fitzer SC, Caldwell GS, Close AJ, Clare AS (2012) Ocean acidification induces multi-generational decline in copepod naupliar production with possible conflict for reproductive resource allocation. J Exp Mar Biol Ecol 418–419:30–36. doi: 10.1016/j.jembe.2012.03.009 CrossRefGoogle Scholar
  31. Garzke J, Ismar SMH, Sommer U (2015) Climate change affects low trophic level marine consumers: warming decreases copepod size and abundance. Oecologia 177:849–860. doi: 10.1007/s00442-014-3130-4 CrossRefPubMedGoogle Scholar
  32. Garzke J, Hansen T, Ismar SMH, Sommer U (2016) Combined effects of ocean warming and acidification on copepod abundance, body size and fatty acid content. PLoS One 11:e0155952. doi: 10.1371/journal.pone.0155952 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Hansen T, Sommer U (2007) Increasing the sensitivity of δ13 C and δ15 N abundance measurements by a high sensitivity elemental analyzer connected to an isotope ratio mass spectrometer. Rapid Commun Mass Sp 21:314–318. doi: 10.1002/rcm.2847 CrossRefGoogle Scholar
  34. Havenhand J, Dupont S, Quinn GP (2010) Designing ocean acidification experiments to maximise inference. In: Riebesell U, Fabry VJ, Hansson L, Gattuso JP (eds) Guide to best practices for ocean acidification research and data reporting. Publications Office of the European Union, Brussels, LuxembourgGoogle Scholar
  35. Hildebrandt N, Niehoff B, Sartoris FJ (2014) Long-term effects of elevated CO2 and temperature on the Arctic calanoid copepods Calanus glacialis and C. hyperboreus. Mar Pollut Bull 80:59–70. doi: 10.1016/j.marpolbul.2014.01.050 CrossRefPubMedGoogle Scholar
  36. Hirche H-J, Niehoff B (1996) Reproduction of the Arctic copepod Calanus hyperboreus in the Greenland Sea-field and laboratory observations. Polar Biol 16:209–219. doi: 10.1007/BF02329209 CrossRefGoogle Scholar
  37. Holste L, Peck MA (2005) The effects of temperature and salinity on egg production and hatching success of Baltic Acartia tonsa (Copepoda: Calanoida): a laboratory investigation. Mar Biol 148:1061–1070. doi: 10.1007/s00227-005-0132-0 CrossRefGoogle Scholar
  38. Ikeda T, Kanno Y, Ozaki K, Shinada A (2001) Metabolic rates of epipelagic marine copepods as a function of body mass and temperature. Mar Biol 139:587–596CrossRefGoogle Scholar
  39. IPCC (2014) Climate Change 2014: Mitigation of Climate Change. Contribution of Working Group III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USAGoogle Scholar
  40. Kordas RL, Harley CDG, O’Connor MI (2011) Community ecology in a warming world: the influence of temperature on interspecific interactions in marine systems. J Exp Mar Biol Ecol 400:218–226. doi: 10.1016/j.jembe.2011.02.029 CrossRefGoogle Scholar
  41. Kurihara H (2008) Effects of CO2-driven ocean acidification on the early developmental stages of invertebrates. Mar Ecol Prog Ser 373:275–284. doi: 10.3354/meps07802 CrossRefGoogle Scholar
  42. 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. doi: 10.1016/j.marpolbul.2008.03.023 CrossRefPubMedGoogle Scholar
  43. Kurihara H, Shimode S, Shirayama Y (2004) Effects of raised CO2 concentration on the egg production rate and early development of two marine copepods (Acartia steueri and Acartia erythraea). Mar Pollut Bull 49:721–727. doi: 10.1016/j.marpolbul.2004.05.005 CrossRefPubMedGoogle Scholar
  44. Leandro SM, Queiroga H, Rodriguez-Grana L, Tiselius P (2006) Temperature-dependent development and somatic growth in two allopatric populations of Acartia clausi (Copepoda : Calanoida). Mar Ecol Prog Ser 322:189–197CrossRefGoogle Scholar
  45. Lennartz ST, Lehmann A, Herrford J et al (2014) Long-term trends at the Boknis Eck time series station (Baltic Sea), 1957–2013: does climate change counteract the decline in eutrophication? Biogeosciences 11:6323–6339. doi: 10.5194/bg-11-6323-2014 CrossRefGoogle Scholar
  46. Longhurst AR (1985) The structure and evolution of plankton communities. Prog Oceanogr 15:1–35. doi: 10.1016/0079-6611(85)90036-9 CrossRefGoogle Scholar
  47. Mackas DL, Greve W, Edwards M et al (2012) Changing zooplankton seasonality in a changing ocean: Comparing time series of zooplankton phenology. Prog Oceanogr 97:31–62CrossRefGoogle Scholar
  48. Malzahn AM, Boersma M (2012) Effects of poor food quality on copepod growth are dose dependent and non-reversible. Oikos 121:1408–1416. doi: 10.1111/j.1600-0706.2011.20186.x CrossRefGoogle Scholar
  49. Malzahn AM, Aberle N, Clemmensen C, Boersma M (2007) Nutrient limitation of primary producers affects planktivorous fish condition. Limnol Oceanogr 52:2062–2071CrossRefGoogle Scholar
  50. Malzahn AM, Hantzsche F, Schoo KL et al (2010) Differential effects of nutrient-limited primary production on primary, secondary or tertiary consumers. Oecologia 162:35–48. doi: 10.1007/s00442-009-1458-y CrossRefPubMedGoogle Scholar
  51. Mayor DJ, Anderson TR, Pond DW, Irigoien X (2009) Egg production and associated losses of carbon, nitrogen and fatty acids from maternal biomass in Calanus finmarchicus before the spring bloom. J Mar Sys 78:505–510. doi: 10.1016/j.jmarsys.2008.12.019 CrossRefGoogle Scholar
  52. Mayor DJ, Everett NR, Cook KB (2012) End of century ocean warming and acidification effects on reproductive success in a temperate marine copepod. J Plankton Res 34:258–262. doi: 10.1093/plankt/fbr107 CrossRefGoogle Scholar
  53. Mayor DJ, Sommer U, Cook KB, Viant MR (2015) The metabolic response of marine copepods to environmental warming and ocean acidification in the absence of food. Sci Rep. doi: 10.1038/srep13690 Google Scholar
  54. Möllmann C, Kornilovs G, Fetter M, Köster FW (2005) Climate, zooplankton, and pelagic fish growth in the central Baltic Sea. ICES J Mar Sci 62:1270–1280CrossRefGoogle Scholar
  55. Müller-Navarra DC (2008) Food web paradigms: the biochemical view on trophic interactions. Int Rev Hydrobiol 93:489–505. doi: 10.1002/iroh.200711046 CrossRefGoogle Scholar
  56. Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42. doi: 10.1038/nature01286 CrossRefPubMedGoogle Scholar
  57. Paul C, Matthiessen B, Sommer U (2015) Warming but not enhanced CO2 quantitatively and qualitatively affects phytoplankton biomass. Mar Ecol Prog Ser. doi: 10.3354/meps11264 Google Scholar
  58. Paul C, Sommer U, Garzke J et al (2016) Effects of increased CO2 concentration on nutrient limited coastal summer plankton depend on temperature. Limnol Oceanogr 61:853–868. doi: 10.1002/lno.10256 CrossRefGoogle Scholar
  59. Pedersen SA, Hansen BH, Altin D, Olsen AJ (2013) Medium-term exposure of the North Atlantic copepod Calanus finmarchicus (Gunnerus, 1770) to CO2-acidified seawater: effects on survival and development. Biogeosciences 10:7481–7491. doi: 10.5194/bg-10-7481-2013 CrossRefGoogle Scholar
  60. Pedersen SA, Håkedal OJ, Salaberria I et al (2014) Multigenerational exposure to ocean acidification during food limitation reveals consequences for copepod scope for growth and vital rates. Environ Sci Technol 48:12275–12284. doi: 10.1021/es501581j CrossRefPubMedGoogle Scholar
  61. Pierrot D, Lewis E, Wallace D (2006) MS Excel program developed for CO2 system calculations: ORNL/CDIAC-105a. Carbon Dioxide Information Analysis Centre Oak Ridge National Laboratory, US Department of Energy, Oak Rodge, TennesseeGoogle Scholar
  62. Plath K, Boersma M (2001) Mineral limitation of zooplankton: stoichiometric constraints and optimal foraging. Ecology 82:1260–1269. doi: 10.1890/0012-9658(2001)082[1260:mlozsc]2.0.co;2 CrossRefGoogle Scholar
  63. Pörtner HO, Farrell AP (2008) Ecology: physiology and climate change. Science 322:690–692. doi: 10.1126/science.1163156 CrossRefPubMedGoogle Scholar
  64. Pörtner HO, Langenbuch M, Reipschläger A (2004) Biological impact of elevated ocean CO2 concentrations: lessons from animal physiology and earth history. J Oceanogr 60:705–718. doi: 10.1007/s10872-004-5763-0 CrossRefGoogle Scholar
  65. Przeslawski R, Byrne M, Mellin C (2015) A review and meta-analysis of the effects of multiple abiotic stressors on marine embryos and larvae. Glob Change Biol 21:2122–2140. doi: 10.1111/gcb.12833 CrossRefGoogle Scholar
  66. Rice E, Dam HG, Stewart G (2014) Impact of climate change on estuarine zooplankton: surface water warming in long island sound is associated with changes in copepod size and community structure. Estuar Coasts. doi: 10.1007/s12237-014-9770-0 Google Scholar
  67. Richardson AJ (2004) Climate impact on plankton ecosystems in the northeast Atlantic. Science 305:1609–1612. doi: 10.1126/science.1100958 CrossRefPubMedGoogle Scholar
  68. Richardson AJ (2008) In hot water: zooplankton and climate change. ICES J Mar Sci 65:279–295. doi: 10.1093/icesjms/fsn028 CrossRefGoogle Scholar
  69. Schoo KL, Malzahn AM, Krause E, Boersma M (2013) Increased carbon dioxide availability alters phytoplankton stoichiometry and affects carbon cycling and growth of a marine planktonic herbivore. Mar Biol 160:2145–2155. doi: 10.1007/s00227-012-2121-4 CrossRefGoogle Scholar
  70. Schulz KG, Bellerby RGJ, Brussaard CPD et al (2013) Temporal biomass dynamics of an Arctic plankton bloom in response to increasing levels of atmospheric carbon dioxide. Biogeosciences 10:161–180. doi: 10.5194/bg-10-161-2013 CrossRefGoogle Scholar
  71. Sommer U, Sommer F (2005) Cladocerans versus copepods: the cause of contrasting top–down controls on freshwater and marine phytoplankton. Oecologia 147:183–194. doi: 10.1007/s00442-005-0320-0 CrossRefPubMedGoogle Scholar
  72. Speekmann CL, Hyatt CJ, Buskey EJ (2006a) Effects of Karenia brevis diet on RNA:DNA ratios and egg production of Acartia tonsa. Harmful Algae 5:693–704. doi: 10.1016/j.hal.2006.03.002 CrossRefGoogle Scholar
  73. Speekmann CL, Nunez BS, Buskey EJ (2006b) Measuring RNA:DNA ratios in individual Acartia tonsa (Copepoda). Mar Biol 151:759–766. doi: 10.1007/s00227-006-0520-0 CrossRefGoogle Scholar
  74. Sterner RW (2010) Role of Zooplankton in Aquatic Ecosystems. In: Likens GE (ed) Encyclopedia of inland waters, 1st edn. Elsevier, Oxford, UK, pp 678–688Google Scholar
  75. Sterner RW, Elser JJ (2002) Ecological stochiometry: the biology of elements from molecules to the biosphere. Princeton University Press, New JerseyGoogle Scholar
  76. Stocker TF, Quin D, Plattner GH et al (2013) IPCC, 2013: Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge, United KingdomGoogle Scholar
  77. Thomsen J, Gutowska MA, Saphorster J 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. doi: 10.5194/bg-7-3879-2010 CrossRefGoogle Scholar
  78. Thor P, Dupont S (2015) Transgenerational effects alleviate severe fecundity loss during ocean acidification in a ubiquitous planktonic copepod. Glob Change Biol 21:2261–2271. doi: 10.1111/gcb.12815 CrossRefGoogle Scholar
  79. Urabe J, Togari JUN, Elser JJ (2003) Stoichiometric impacts of increased carbon dioxide on a planktonic herbivore. Glob Change Biol 9:818–825. doi: 10.1046/j.1365-2486.2003.00634.x CrossRefGoogle Scholar
  80. Vehmaa A, Brutemark A, Engstrom-Ost J (2012) Maternal effects may act as an adaptation mechanism for copepods facing ph and temperature changes. PLoS One. doi: 10.1371/journal.pone.0048538 PubMedPubMedCentralGoogle Scholar
  81. Vehmaa A, Almén AK, Brutemark A (2015) Ocean acidification challenges copepod reproductive plasticity. Biogeosciences 12:18541–18570CrossRefGoogle Scholar
  82. Whiteley NM (2011) Physiological and ecological responses of crustaceans to ocean acidification. Mar Ecol Prog Ser 430:257–271. doi: 10.3354/meps09185 CrossRefGoogle Scholar
  83. Zervoudaki S, Frangoulis C, Giannoudi L, Krasakopoulou E (2014) Effects of low pH and raised temperature on egg production, hatching and metabolic rates of a Mediterranean copepod species (Acartia clausi) under oligotrophic conditions. Mediterr Mar Sci 15:74–83CrossRefGoogle Scholar
  84. Zhang D, Li S, Wang G, Guo D (2011) Impacts of CO2-driven seawater acidification on survival, egg production rate and hatching success of four marine copepods. Acta Oceanol Sin 30:86–94. doi: 10.1007/s13131-011-0165-9 CrossRefGoogle Scholar

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© Springer International Publishing 2017

Authors and Affiliations

  1. 1.Department Experimental Ecology, Food WebsGeomar Helmholtz Centre for Ocean Research KielKielGermany

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