Species and gamete-specific fertilization success of two sea urchins under near future levels of pCO2

Abstract Since the Industrial Revolution, rising atmospheric CO 2 concentration has driven an increase in the partial pressure of CO 2 in seawater ( p CO 2 ), thus lowering ocean pH. We examined the separate effects of exposure of gametes to elevated p CO 2 and low pH on fertilization success of the sea urchin Strongylocentrotus nudus . Sperm and eggs were independently exposed to seawater with p CO 2 levels ranging from 380 (pH 7.96–8.3) to 6000 ppmv (pH 7.15–7.20). When sperm were exposed, fertilization rate decreased drastically with increased p CO 2 , even at a concentration of 450 ppmv (pH range: 7.94 to 7.96). Conversely, fertilization of Hemicentrotus pulcherrimus was not significantly changed even when sperm was exposed to p CO2 concentrations as high as 750 ppmv. Exposure of S. nudus eggs to seawater with high p CO 2 did not affect fertilization success, suggesting that the effect of increased p CO 2 on sperm is responsible for reduced fertilization success. Surprisingly, this result was not related to sperm motility, which was insensitive to p CO 2 . When seawater was acidified using HCl, leaving p CO 2 constant, fertilization success in S. nudus remained high (> 80%) until pH decreased to 7.3. While further studies are required to elucidate the physiological mechanism by which elevated p CO 2 impairs sperm and reduces S. nudus fertilization, this study suggests that in the foreseeable future, sea urchin survival may be threatened due to lower fertilization success driven by elevated p CO 2 rather than by decreased pH in seawater.

[1]  N. Emery,et al.  Jackdaws Respond to Human Attentional States and Communicative Cues in Different Contexts , 2009, Current Biology.

[2]  M. Saier,et al.  Climate Change, 2007 , 2007 .

[3]  K. Caldeira,et al.  Oceanography: Anthropogenic carbon and ocean pH , 2003, Nature.

[4]  M. Byrne,et al.  A boom–bust phylum? Ecological and evolutionary consequences of density variations in echinoderms , 2009 .

[5]  U. Riebesell,et al.  Enhanced biological carbon consumption in a high CO2 ocean , 2006, Nature.

[6]  M. Byrne,et al.  Fertilization in a suite of coastal marine invertebrates from SE Australia is robust to near-future ocean warming and acidification , 2010 .

[7]  E. Maier‐Reimer,et al.  Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms , 2005, Nature.

[8]  H. Kurihara,et al.  Effects of elevated pCO2 on early development in the mussel Mytilus galloprovincialis , 2008 .

[9]  P. Schlegel,et al.  Near-future levels of ocean acidification do not affect sperm motility and fertilization kinetics in the oyster Crassostrea gigas , 2009 .

[10]  S. Dupont,et al.  What meta-analysis can tell us about vulnerability of marine biodiversity to ocean acidification? , 2010 .

[11]  J. Rotchell,et al.  Analytical challenges and the development of biomarkers to measure and to monitor the effects of ocean acidification , 2011 .

[12]  S. Dupont,et al.  Impact of near-future ocean acidification on echinoderms , 2010, Ecotoxicology.

[13]  Toby Tyrrell,et al.  Phytoplankton Calcification in a High-CO2 World , 2008, Science.

[14]  Maria Byrne,et al.  Temperature, but not pH, compromises sea urchin fertilization and early development under near-future climate change scenarios , 2009, Proceedings of the Royal Society B: Biological Sciences.

[15]  S. Solomon.  The Physical Science Basis : Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change , 2007 .

[16]  N. Nakabayashi,et al.  Food of the sea urchins Strongylocentrotus nudus and Hemicentrotus pulcherrimus associated with vertical distributions in fucoid beds and crustose coralline flats in northern Honshu, Japan , 2007 .

[17]  K. Lotterhos,et al.  Elevated pCO2 increases sperm limitation and risk of polyspermy in the red sea urchin Strongylocentrotus franciscanus , 2011 .

[18]  M. Thorndyke,et al.  Near-future levels of ocean acidificat ion reduce fert ilizat ion success in a sea urchin , 2018 .

[19]  H. Kubo,et al.  Sperm Motility-Initiating Activity in the Egg Jelly of the Externally-Fertilizing Urodele Amphibian, Hynobius lichenatus , 2010, Zoological science.

[20]  W. O'Connor,et al.  Comparing the effect of elevated pCO2 and temperature on the fertilization and early development of two species of oysters , 2010 .

[21]  M. Gillings,et al.  Individual Variability in Reproductive Success Determines Winners and Losers under Ocean Acidification: A Case Study with Sea Urchins , 2012, PloS one.

[22]  Y. Shirayama,et al.  Effects of increased atmospheric CO2 on sea urchin early development , 2004 .

[23]  J. Pechenik.  On the advantages and disadvantages of larval stages in benthic marine invertebrate life cycles , 1999 .

[24]  R. Feely,et al.  Evidence for Upwelling of Corrosive "Acidified" Water onto the Continental Shelf , 2008, Science.

[25]  S. Morley,et al.  The response of two ecologically important Antarctic invertebrates (Sterechinus neumayeri and Parborlasia corrugatus) to reduced seawater pH: effects on fertilisation and embryonic development , 2010 .

[26]  W. O'Connor,et al.  The effect of ocean acidification and temperature on the fertilization and embryonic development of the Sydney rock oyster Saccostrea glomerata (Gould 1850) , 2009 .

[27]  J. Link,et al.  Improved methodology for a sea urchin sperm cell bioassay for marine waters , 1987, Archives of environmental contamination and toxicology.

[28]  Christopher D G Harley,et al.  The impacts of climate change in coastal marine systems. , 2006, Ecology letters.

[29]  J. Largier,et al.  Observations of increased wind‐driven coastal upwelling off central California , 2010 .

[30]  F. Micheli,et al.  The effects of intermittent exposure to low-pH and low-oxygen conditions on survival and growth of juvenile red abalone , 2013 .

[31]  Andrew S. Brierley,et al.  Impacts of Climate Change on Marine Organisms and Ecosystems , 2009, Current Biology.

[32]  G. Thorson.  REPRODUCTIVE and LARVAL ECOLOGY OF MARINE BOTTOM INVERTEBRATES , 1950, Biological reviews of the Cambridge Philosophical Society.

[33]  Gerald G Singh,et al.  Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. , 2010, Ecology letters.

[34]  Claire B Paris-Limouzy,et al.  Connectivity of marine populations: open or closed? , 2000, Science.

[35]  N. Kobayashi.  FERTILIZED SEA URCHIN EGGS AS AN INDICATORY MATERIAL FOR MARINE POLLUTION BIOASSAY, PRELIMINARY EXPERIMENTS , 1971 .

[36]  C. Langdon,et al.  Ocean acidification compromises recruitment success of the threatened Caribbean coral Acropora palmata , 2010, Proceedings of the National Academy of Sciences.

[37]  R. Carr,et al.  Influence of Potentially Confounding Factors on Sea Urchin Porewater Toxicity Tests , 2006, Archives of environmental contamination and toxicology.

[38]  J. Havenhand,et al.  Barriers to Cross-Fertilization Between Populations of a Widely Dispersed Polychaete Species are Unlikely to Have Arisen Through Gametic Compatibility Arms-Races , 2008, Evolution; international journal of organic evolution.

[39]  A. Grace,et al.  Intracellular pH recovery during respiratory acidosis in perfused hearts. , 1994, The American journal of physiology.

[40]  M. Byrne,et al.  Beyond corals and fish: the effects of climate change on noncoral benthic invertebrates of tropical reefs , 2008 .

[41]  Robert W. Buddemeier,et al.  Ocean biogeochemistry: Calcification and CO2 , 2000, Nature.

[42]  Andrew J. Watson,et al.  Ocean acidification due to increasing atmospheric carbon dioxide , 2005 .

[43]  Adina Paytan,et al.  High-Frequency Dynamics of Ocean pH: A Multi-Ecosystem Comparison , 2011, PloS one.

[44]  Yaqing Chang,et al.  Evaluation of the growth and heterosis of hybrids among three commercially important sea urchins in China: Strongylocentrotus nudus, S. intermedius and Anthocidaris crassispina , 2007 .

[45]  Andrew R. Davis,et al.  Impact of Ocean Warming and Ocean Acidification on Larval Development and Calcification in the Sea Urchin Tripneustes gratilla , 2010, PloS one.

[46]  Gary S. Caldwell,et al.  Ocean acidification takes sperm back in time , 2011 .

[47]  Takashi Kikkawa,et al.  Comparison of the lethal effect of CO2 and acidification on red sea bream (Pagrus major) during the early developmental stages. , 2004, Marine pollution bulletin.

[48]  M. Byrne,et al.  Unshelled abalone and corrupted urchins: development of marine calcifiers in a changing ocean , 2011, Proceedings of the Royal Society B: Biological Sciences.

[49]  R. E. Nakatani,et al.  Development of a sperm cell toxicity test for marine waters , 1982 .

[50]  J. Gatti,et al.  Rapid and quantitative assessment of trout spermatozoa motility using stroboscopy , 1985 .

[51]  Elizabeth J. Bailey,et al.  The Impact of Ocean Acidification on Reproduction, Early Development and Settlement of Marine Organisms , 2011 .

[52]  Effects of increased atmospheric CO2 and decreased pH on sea urchin embryos and gametes , 2004 .

[53]  Robert W. Buddemeier,et al.  Calcification and CO 2 , 2000 .

[54]  M. Byrne,et al.  Sea urchin fertilization in a warm, acidified and high pCO2 ocean across a range of sperm densities. , 2010, Marine environmental research.

[55]  C. Brokaw.  CO2-inhibition of the amplitude of bending of triton-demembranated sea urcin sperm flagella. , 1977, The Journal of experimental biology.

[56]  K. Inaba,et al.  Control of flatfish sperm motility by CO2 and carbonic anhydrase. , 2003, Cell motility and the cytoskeleton.