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Effects of pH and temperature on egg hatching success of the marine planktonic copepod, Calanus finmarchicus

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Abstract

Calanus finmarchicus is a predominant planktonic copepod in the northern North Atlantic Ocean, where it is a fundamental link in the transfer of energy from phytoplankton to fish. Here, we investigate whether ocean acidification at present-day and future levels will cause a significant decrease in the egg hatching success (HS) of C. finmarchicus in the Gulf of Maine. Eggs spawned by female C. finmarchicus collected from the coastal Gulf of Maine were incubated in seawater acidified by addition of CO2 to selected pH levels at 3.5 °C (in a single experiment), 6 °C and 14–15 °C (in multiple experiments). HS was unaffected by pH between 6.58 and 8.0 at 3.5 and 6 °C, and between 7.1 and 8.0 when incubated at 15 °C. A significant interactive effect between temperature and pH on HS was found using a two-way ANOVA of the data from experiments at 6 °C and 14–15 °C, temperatures that are experienced in summer in the Gulf of Maine. HS of eggs spawned from C. finmarchicus females immediately after capture from a coastal station was significantly reduced at pH ≤ 7.0 when incubated at 14–15 °C, although HS of eggs collected from well-fed females in the laboratory in water from the Damariscotta Estuary was not significantly reduced at pH levels as low as 6.6 at 15 °C. This finding is consistent with the hypothesis that parental history and possibly maternal provisioning can influence capability of eggs to adjust to lower pH environments. While an interaction between pH and temperatures experienced by C. finmarchicus at the southern edge of its biogeographic range was observed, the pH at which this interaction occurred is substantially lower than pH levels predicted for the surface ocean over the surface ocean.

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References

  • Armstrong RA (2014) When to use the Bonferroni correction. Ophthalmic Physiol Opt 34:502–508

    Article  Google Scholar 

  • Armstrong FAJ, Stearns CR, Strickland JDH (1967) The measurement of upwelling and subsequent biological processes by means of the Technicon autoanalyzer and associated equipment. Deep Sea Res 14:381–389

    CAS  Google Scholar 

  • Bailey A, Thor P, Browman HI, Fields DM, Runge J, Vermont A, Bjelland R, Thompson C, Shema S, Durif CMF, Hop H (2017) Early life stages of the Arctic copepod Calanus glacialis are unaffected by increased seawater pCO2. ICES J Mar Sci 74(4):996–1004

  • Breitburg DL, Salisbury J, Bernhard JM, Cai WJ, Dupont S, Doney SC, Kroeker KJ, Levin LA, Long WC, Milke LM, Miler SH, Phelan B, Passow U, Seibel BA, Todgham AE, Tarrant AM (2015) And on top of all that… Coping with ocean acidification in the midst of many stressors. Oceanography 28:48–61

    Article  Google Scholar 

  • Caldeira K,Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425:365

    Article  CAS  Google Scholar 

  • Campbell RG, Wagner MM, Teegarden GJ, Boudreau CA, Durbin EG (2001) Growth and development rates of the copepod Calanus finmarchicus reared in the laboratory. Mar Ecol Prog Ser 221:161–183

    Article  Google Scholar 

  • Christensen JP (2008) Sedimentary carbon oxidation and denitrification on the shelf break of the Alaskan Beaufort and Chukchi Seas. Open Oceanogr 2:6–17

    Article  CAS  Google Scholar 

  • Cripps G, Lindeque P, Flynn K (2014a) Parental exposure to elevated pCO2 influences the reproductive success of copepods. J Plankton Res 36:1165–1174

    Article  CAS  Google Scholar 

  • Cripps G, Lindeque P, Flynn KJ (2014b) Have we been underestimating the effects of ocean acidification in zooplankton? Glob Change Biol 20:3377–3385

    Article  Google Scholar 

  • Dickson AG (1990a) Thermodynamics of the dissociation of boric acid in synthetic sea water from 273.15 to 298.15 K. Deep Sea Res 37:755–766

    Article  CAS  Google Scholar 

  • Dickson AG (1990b) Standard potential of the reaction: AgCl(s) + 1/2 H2(g) = Ag(s) + HCl(aq), and the standard acidity constant of the ion HSO4 in synthetic seawater from 273.15 to 318.15 K. J Chem Thermodyn 22:113–127

    Article  CAS  Google Scholar 

  • Dickson AG, Riley JP (1979) The estimation of acid dissociation constants in seawater media from potentiometric titrations with strong base. II. The dissociation of phosphoric acid. Mar Chem 7:101–109

    Article  CAS  Google Scholar 

  • Dickson AG, Sabine CL, Christian JR (2007) Guide to best practices for ocean CO2 measurements. PICES Spec Publ 3:191

    Google Scholar 

  • DOE (1994) Handbook of methods for the analysis of the various parameters of the carbon dioxide system in sea water; version 2. In: Dickson AG, Goyet C (eds) ORNL/CDIAC-74

  • Doney S (2009) The consequences of human-driven ocean acidification for marine life. F1000 Biol Rep 1:7–10

    Article  Google Scholar 

  • Drummond L, Maher W (1995) Determination of phosphorus in aqueous solution via formation of the phosphoantimonylmolybdenum blue complex. Re-examination of optimum conditions for the analysis of phosphate. Anal Chim Acta 302:69–74

    Article  CAS  Google Scholar 

  • Fabry VJ, Seibel BA, Feely RA, Orr JC (2008) Impacts of ocean acidification on marine fauna and ecosystem processes. ICES J Mar Sci Journal du Conseil 65:414–432

    Article  CAS  Google Scholar 

  • Feely R, Doney SC, Cooley S (2009) Ocean acidification: present conditions and future changes in a high-CO2 world. J Acoust Soc Am 22:36–47

    Google Scholar 

  • 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(5):e0155952. doi:10.1371/journal.pone.0155952

    Article  Google Scholar 

  • Guillard R, Ryther J (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt, and Detonula confervacea (cleve) Gran. Can J Microbiol 8:229–239

    Article  CAS  Google Scholar 

  • IPCC (2014) Climate change 2014: synthesis report. In: Core Writing Team, Pachauri RK, Meyer LA (eds) Contribution of Working Groups I, II and III to the fifth assessment report of the intergovernmental panel on climate change. IPCC, Geneva, Switzerland, 151 p

  • Johnson CL, Runge JA, Curtis KA, Durbin EG, Hare JA, Incze LS, Link JS, Melvin GD, O’Brien TD, Guelpen LV (2011) Biodiversity and ecosystem function in the Gulf of Maine: pattern and role of zooplankton and pelagic nekton. PLoS One 6:1–18

    Google Scholar 

  • Koroleff F (1970) Revised version of “Direct determination of ammonia in natural waters as indophenol blue, Int. Con. Explor. Sea, C.M. 1969/C:9”. ICES Information on Techniques and Methods for Sea Water Analysis Interlab Rep No. 3, pp 19–22

  • 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(6):1086–1090

    Article  CAS  Google Scholar 

  • Kurihara H, Shirayama Y (2004) Effects of increased atmospheric CO2 on sea urchin early development. Mar Ecol Prog Ser 274:161–169

    Article  Google Scholar 

  • 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(9):721–727

    Article  CAS  Google Scholar 

  • Lewis ER, Wallace DWR (1995) Basic programs for the CO2 system in seawater. BNL-61827. Brookhaven National Laboratory, Upton, p 11973

    Book  Google Scholar 

  • Marshall SM, Orr AP (1972) The biology of a marine copepod. Springer, Berlin

    Book  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • McConville K, Halsband C, Fileman ES, Somerfield PJ, Findlay HS, Spicer JI (2013) Effects of elevated CO2 on the reproduction of two calanoid copepods. Mar Pollut Bull 73:428–434

    Article  CAS  Google Scholar 

  • McLaren IA, Corkett CJ, Zillioux EJ (1969) Temperature adaptations of copepod eggs from the arctic to the tropics. Biol Bull 137:486–493

    Article  Google Scholar 

  • Melle W, Runge JA, Head E, Plourde S, Castellani C, Licandro P, Pierson J, Jónasdóttir SH, Johnson C, Broms C, Debes H, Falkenhaug T, Gaard E, Gislason A, Heath M, Niehoff B, Nielsen TG, Pepin P, Stenevik EK, Chust G (2014) The North Atlantic Ocean as habitat for zooplankton: distribution of key taxa in relation to environmental factors and ecological traits, with a focus on the planktonic copepod, Calanus finmarchicus. Prog Oceanogr 129:244–284

    Article  Google Scholar 

  • Millero FJ (1995) Thermodynamics of the carbon dioxide system in the oceans. Geochim et Cosmochimica Ac 59:661–677

    Article  CAS  Google Scholar 

  • Mills KE, Pershing AJ, Brown CJ (2013) Fisheries management in a changing climate: lessons from the 2012 ocean heat wave in the Northwest Atlantic. Oceanography 26:191–195

    Article  Google Scholar 

  • Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, Feely RA, Gnanadesikan A, Gruber N, Ishida A, Joos F, Key RM, Lindsay K, Maier-Reimer E, Matear R, Monfray P, Mouchet A, Najjar RG, Plattner G, Rodgers KB, Sabine CL, Sarmiento JL, Schliltzer R, Slater RD, Totterdell IJ, Weirig M, Yamanaka Y, Yool A (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437:681–686

    Article  CAS  Google Scholar 

  • Pavlou SP (1972) Phytoplankton growth dynamics. Technical series 1, chemostat methodology and chemical analyses. Special Report No. 52, Dept. of Oceanography, University of Washington, Seattle, WA 98195, p 130

  • Pedersen SA, Våge VT, Olsen AJ, Hammer KM, Altin D (2014a) Effects of elevated carbon dioxide (CO2) concentrations on early developmental stages of the marine copepod Calanus finmarchicus Gunnerus (Copepoda: Calanoidae). J Toxicol Environ Health 77:535–549

    Article  CAS  Google Scholar 

  • Pedersen SA, Håkedal OJ, Salaberria I, Tagliati A, Gustavson LM, Jenssen BM, Altin D (2014b) Multigenerational exposure to ocean acidification during food limitation reveals consequences for copepod scope for growth and vital rates. Environ Sci Technol 48:12275–12284

    Article  CAS  Google Scholar 

  • Pershing AJ, Alexander MA, Hernandez CM, Kerr LA, Le Bris A, Mills KE, Sherwood GD (2015) Slow adaptation in the face of rapid warming leads to collapse of the Gulf of Maine cod fishery. Science 350(6262):809–812

    Article  CAS  Google Scholar 

  • Preziosi BM, Runge JA (2014) The effect of warm temperatures on hatching success of the marine planktonic copepod, Calanus finmarchicus. J Plankton Res 36:1381–1384

    Article  Google Scholar 

  • Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Reygondeau G, Beaugrand G (2011) Future climate-driven shifts in distribution of Calanus finmarchicus. Glob Change Biol 17:756–766

    Article  Google Scholar 

  • Roy RN, Roy LN, Vogel KM, Porter-Moore C, Pearson T, Good CE, Millero FJ, Campbell DM (1993) Determination of the ionization constants of carbonic acid in seawater in salinities 5 to 45 and temperatures 0 to 45 °C. Mar Chem 44:249–267

    Article  CAS  Google Scholar 

  • Runge JA (1985) Relationship of egg production of Calanus pacificus to seasonal changes in phytoplankton availability in Puget Sound, Washington. Limnol Oceanogr 30:382–396

    Article  Google Scholar 

  • Runge JA, Fields DM, Thompson CR, Shema SD, Bjelland RM, Durif CM, Skiftesvik AB, Browman HI (2016) End of the century CO2 concentrations do not have a negative effect on vital rates of Calanus finmarchicus, an ecologically critical planktonic species in North Atlantic ecosystems. ICES J Mar Sci Journal du Conseil 73:937–950

    Article  Google Scholar 

  • Slawyk G, MacIsaac JJ (1972) Comparison of two automated ammonium methods in a region of coastal upwelling. Deep Sea Res 19:521–524

    CAS  Google Scholar 

  • Underwood AJ (1997) Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press, Cambridge

    Google Scholar 

  • UNESCO (1981) Background papers and supporting data on the international equation of state of seawater, 1980. UNESCO Tech Pap Mar Sci 38:193

    Google Scholar 

  • Vehmaa A, Brutemark A, Engström-Öst J (2012) Maternal effects may act as an adaptation mechanism for copepods facing pH and temperature changes. PLoS One 7(10):e48538

    Article  CAS  Google Scholar 

  • Weiss RF (1974) Carbon dioxide in water and seawater: the solubility of a non-ideal gas. Mar Chem 2:203–215

    Article  CAS  Google Scholar 

  • Weydmann A, Søreide JE, Kwasniewski S, Widdicombe S (2012) Influence of CO2-induced acidification on the reproduction of a key Arctic copepod Calanus glacialis. J Exp Mar Biol Ecol 428:39–42

    Article  CAS  Google Scholar 

  • 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. Hai Yang Xue Bao 30:86–94

    CAS  Google Scholar 

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Acknowledgements

This research was supported by National Science Foundation awards OCE-1041081, OCE-1459087 and OCE-1551195. We gratefully acknowledge Michael Devin for assistance with the phytoplankton cultures. We thank three anonymous reviewers for comments that greatly improved the manuscript.

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Correspondence to Jeffrey A. Runge.

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Preziosi, B.M., Runge, J.A., Christensen, J.P. et al. Effects of pH and temperature on egg hatching success of the marine planktonic copepod, Calanus finmarchicus . Mar Biol 164, 218 (2017). https://doi.org/10.1007/s00227-017-3243-5

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