Adult acclimation to combined temperature and pH stressors significantly enhances reproductive outcomes compared to short-term exposures.

This study examined the effects of long-term culture under altered conditions on the Antarctic sea urchin, Sterechinus neumayeri. Sterechinus neumayeri was cultured under the combined environmental stressors of lowered pH (-0.3 and -0.5 pH units) and increased temperature (+2 °C) for 2 years. This time-scale covered two full reproductive cycles in this species and analyses included studies on both adult metabolism and larval development. Adults took at least 6-8 months to acclimate to the altered conditions, but beyond this, there was no detectable effect of temperature or pH. Animals were spawned after 6 and 17 months exposure to altered conditions, with markedly different outcomes. At 6 months, the percentage hatching and larval survival rates were greatest in the animals kept at 0 °C under current pH conditions, whilst those under lowered pH and +2 °C performed significantly less well. After 17 months, performance was not significantly different across treatments, including controls. However, under the altered conditions urchins produced larger eggs compared with control animals. These data show that under long-term culture adult S. neumayeri appear to acclimate their metabolic and reproductive physiology to the combined stressors of altered pH and increased temperature, with relatively little measureable effect. They also emphasize the importance of long-term studies in evaluating effects of altered pH, particularly in slow developing marine species with long gonad maturation times, as the effects of altered conditions cannot be accurately evaluated unless gonads have fully matured under the new conditions.

[1]  L. Peck,et al.  Ocean acidification does not impact shell growth or repair of the Antarctic brachiopod Liothyrella uva (Broderip, 1833) , 2015 .

[2]  L. Peck,et al.  Experimental influence of pH on the early life-stages of sea urchins II: increasing parental exposure times gives rise to different responses , 2014 .

[3]  L. Peck,et al.  Experimental influence of pH on the early life-stages of sea urchins I: different rates of introduction give rise to different responses , 2014 .

[4]  S. Dupont,et al.  Evolution in an acidifying ocean. , 2014, Trends in ecology & evolution.

[5]  L. Peck,et al.  Acclimation and thermal tolerance in Antarctic marine ectotherms , 2014, Journal of Experimental Biology.

[6]  Adriana Giangrande,et al.  Adaptation and acclimatization to ocean acidification in marine ectotherms: an in situ transplant experiment with polychaetes at a shallow CO2 vent system , 2013, Philosophical Transactions of the Royal Society B: Biological Sciences.

[7]  P. Dubois,et al.  Buffer capacity of the coelomic fluid in echinoderms. , 2013, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[8]  M. Thorne,et al.  Identification of molecular and physiological responses to chronic environmental challenge in an invasive species: the Pacific oyster, Crassostrea gigas , 2013, Ecology and evolution.

[9]  S. Dupont,et al.  Long-term and trans-life-cycle effects of exposure to ocean acidification in the green sea urchin Strongylocentrotus droebachiensis , 2013 .

[10]  M. Byrne,et al.  Effects of elevated pCO2 and the effect of parent acclimation on development in the tropical Pacific sea urchin Echinometra mathaei , 2013 .

[11]  B. Tilbrook,et al.  Vulnerability of the calcifying larval stage of the Antarctic sea urchin Sterechinus neumayeri to near‐future ocean acidification and warming , 2013, Global change biology.

[12]  Gregory N. Nishihara,et al.  Effect of ocean acidification on growth, gonad development and physiology of the sea urchin Hemicentrotus pulcherrimus , 2013 .

[13]  B. Gaylord,et al.  Evolutionary change during experimental ocean acidification , 2013, Proceedings of the National Academy of Sciences.

[14]  L. Kapsenberg,et al.  Growth Attenuation with Developmental Schedule Progression in Embryos and Early Larvae of Sterechinus neumayeri Raised under Elevated CO2 , 2013, PloS one.

[15]  P. Munday,et al.  Parental environment mediates impacts of increased carbon dioxide on a coral reef fish , 2012 .

[16]  K. Trübenbach,et al.  Resource allocation and extracellular acid-base status in the sea urchin Strongylocentrotus droebachiensis in response to CO₂ induced seawater acidification. , 2012, Aquatic toxicology.

[17]  L. Peck,et al.  Spatial and temporal variation in the heat tolerance limits of two abundant Southern Ocean invertebrates , 2012 .

[18]  U. Riebesell,et al.  Acclimation to ocean acidification during long‐term CO2 exposure in the cold‐water coral Lophelia pertusa , 2012 .

[19]  P. Dubois,et al.  Acid–base balance and metabolic response of the sea urchin Paracentrotus lividus to different seawater pH and temperatures , 2012, Environmental Science and Pollution Research.

[20]  H. Pörtner,et al.  Adult exposure influences offspring response to ocean acidification in oysters , 2012 .

[21]  P. Munday,et al.  Rapid transgenerational acclimation of a tropical reef fish to climate change , 2012 .

[22]  B. Tilbrook,et al.  Combined effects of two ocean change stressors, warming and acidification, on fertilization and early development of the Antarctic echinoid Sterechinus neumayeri , 2012, Polar Biology.

[23]  C. Harley,et al.  Predicting ecosystem shifts requires new approaches that integrate the effects of climate change across entire systems , 2012, Biology Letters.

[24]  P. Dubois,et al.  Sea urchin Arbacia dufresnei (Blainville 1825) larvae response to ocean acidification , 2012, Polar Biology.

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

[26]  L. Peck Organisms and responses to environmental change. , 2011, Marine genomics.

[27]  S. Dupont,et al.  CO2 induced seawater acidification impacts sea urchin larval development I: elevated metabolic rates decrease scope for growth and induce developmental delay. , 2011, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[28]  Steve Widdicombe,et al.  Impact of CO2-acidified seawater on the extracellular acid–base balance of the northern sea urchin Strongylocentrotus dröebachiensis , 2011 .

[29]  F. Micheli,et al.  Divergent ecosystem responses within a benthic marine community to ocean acidification , 2011, Proceedings of the National Academy of Sciences.

[30]  A. Devries,et al.  Heat tolerance and its plasticity in Antarctic fishes. , 2011, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[31]  C. Sweeney,et al.  Short Note: Natural seasonal variability of aragonite saturation state within two Antarctic coastal ocean sites , 2011, Antarctic Science.

[32]  Ulf Riebesell,et al.  Guide to best practices for ocean acidification research and data reporting , 2011 .

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

[34]  L. Peck,et al.  Seasonal physiology and ecology of Antarctic marine benthic predators and scavengers , 2010 .

[35]  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 .

[36]  R. Feely,et al.  Global contribution of echinoderms to the marine carbon cycle: CaCO3 budget and benthic compartments , 2010 .

[37]  L. Peck,et al.  Poor acclimation capacities in Antarctic marine ectotherms , 2010 .

[38]  G. Somero,et al.  The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine ‘winners’ and ‘losers’ , 2010, Journal of Experimental Biology.

[39]  G. R. E T C H E N,et al.  Antarctic echinoids and climate change : a major impact on the brooding forms , 2010 .

[40]  A. Wulff,et al.  Drivers of colonization and succession in polar benthic macro- and microalgal communities , 2009 .

[41]  S. Dupont,et al.  Physiological basis for high CO2 tolerance in marine ectothermic animals: pre-adaptation through lifestyle and ontogeny? , 2009 .

[42]  L. Peck,et al.  Animal temperature limits and ecological relevance: effects of size, activity and rates of change , 2009 .

[43]  D. Clark,et al.  Response of sea urchin pluteus larvae (Echinodermata: Echinoidea) to reduced seawater pH: a comparison among a tropical, temperate, and a polar species , 2009 .

[44]  K. Døving,et al.  Ocean acidification impairs olfactory discrimination and homing ability of a marine fish , 2009, Proceedings of the National Academy of Sciences.

[45]  H. Pörtner Ecosystem effects of ocean acidification in times of ocean warming: a physiologist’s view , 2008 .

[46]  Richard J. Matear,et al.  Southern Ocean acidification: A tipping point at 450-ppm atmospheric CO2 , 2008, Proceedings of the National Academy of Sciences.

[47]  Benjamin S Halpern,et al.  Interactive and cumulative effects of multiple human stressors in marine systems. , 2008, Ecology letters.

[48]  W. Davison,et al.  Antarctic fish can survive prolonged exposure to elevated temperatures , 2008 .

[49]  M. I. Wallace,et al.  Seasonal and interannual variability in temperature, chlorophyll and macronutrients in northern Marguerite Bay, Antarctica. , 2008 .

[50]  Stephen Widdicombe,et al.  Ocean acidification may increase calcification rates, but at a cost , 2008, Proceedings of the Royal Society B: Biological Sciences.

[51]  V. Fabry,et al.  Ocean Acidification and Its Potential Effects on Marine Ecosystems , 2008, Annals of the New York Academy of Sciences.

[52]  S. Widdicombe,et al.  Impact of CO2-induced seawater acidification on the burrowing activity of Nereis virens and sediment nutrient flux , 2007 .

[53]  P. Tyler,et al.  Gametogenesis and gonad mass cycles in the common circumpolar Antarctic echinoid Sterechinus neumayeri , 2007 .

[54]  L. Peck,et al.  Antarctic sessile marine benthos: colonisation and growth on artificial substrata over three years , 2006 .

[55]  J. Gutt,et al.  The genus Sterechinm (Echinodermata: Echinoidea) on the Weddell Sea shelf and slope (Antarctica): distribution, abundance and biomass , 1991, Polar Biology.

[56]  L. Baseh Growth and production of Sterechinus neumayeri ( Echinoidea : Echinodermata ) in McMurdo Sound , Antarctica , 2004 .

[57]  Michael D. Abràmoff,et al.  Image processing with ImageJ , 2004 .

[58]  P. Bouchard,et al.  Time course of the response of mitochondria from oxidative muscle during thermal acclimation of rainbow trout, Oncorhynchus mykiss , 2003, Journal of Experimental Biology.

[59]  T. Piersma,et al.  Phenotypic flexibility and the evolution of organismal design , 2003 .

[60]  Thom Nickell,et al.  Bioturbation, sediment fluxes and benthic community structure around a salmon cage farm in Loch Creran, Scotland , 2003 .

[61]  L. Peck,et al.  Temperature effects on the metabolism of larvae of the Antarctic starfish Odontaster validus, using a novel micro-respirometry method , 2002 .

[62]  Eva Ramirez Llodra Fecundity and life-history strategies in marine invertebrates. , 2002, Advances in marine biology.

[63]  M. Kelly Environmental parameters controlling gametogenesis in the echinoid Psammechinus miliaris , 2001 .

[64]  L. Peck,et al.  Seasonality of respiration and ammonium excretion in the Antarctic echinoid Sterechinus neumayeri , 2001 .

[65]  S. Brockington The seasonal ecology and physiology of Sterechinus neumayeri (Echinodermata: Echinoidea) at Adelaide Island, Antarctica , 2001 .

[66]  H. Pörtner,et al.  Modulation of the cost of pHi regulation during metabolic depression: a (31)P-NMR study in invertebrate (Sipunculus nudus) isolated muscle. , 2000, The Journal of experimental biology.

[67]  J. Mckenzie,et al.  Morphology and survivorship of larval Psammechinus miliaris (Gmelin) (Echinodermata: Echinoidea) in response to varying food quantity and quality , 2000 .

[68]  C. Young,et al.  Temperature and pressure tolerances of embryos and larvae of the Antarctic sea urchin Sterechinus neumayeri (Echinodermata : Echinoidea) : potential for deep-sea invasion from high latitudes , 2000 .

[69]  L. Mcedward,et al.  Body form and skeletal morphometrics during larval development of the sea urchin Lytechinus variegatus Lamarck , 1999 .

[70]  L. Peck,et al.  Temperature and Embryonic Development in Relation to Spawning and Field Occurrence of Larvae of Three Antarctic Echinoderms. , 1998, The Biological bulletin.

[71]  O. Hoegh‐Guldberg,et al.  EFFECTS OF EGG SIZE ON POSTLARVAL PERFORMANCE: EXPERIMENTAL EVIDENCE FROM A SEA URCHIN. , 1997 .

[72]  O. Hoegh‐Guldberg,et al.  EFFECTS OF EGG SIZE ON POSTLARVAL PERFORMANCE: EXPERIMENTAL EVIDENCE FROM A SEA URCHIN , 1997, Evolution; international journal of organic evolution.

[73]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[74]  D. Levitan The Importance of Sperm Limitation to the Evolution of Egg Size in Marine Invertebrates , 1993, The American Naturalist.

[75]  F. Millero,et al.  A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media , 1987 .

[76]  J. Pearse,et al.  DEVELOPMENT, METAMORPHOSIS, AND SEASONAL ABUNDANCE OF EMBRYOS AND LARVAE OF THE ANTARCTIC SEA URCHIN STERECHINUS NEUMAYERI. , 1987, The Biological bulletin.

[77]  C. Culberson,et al.  MEASUREMENT OF THE APPARENT DISSOCIATION CONSTANTS OF CARBONIC ACID IN SEAWATER AT ATMOSPHERIC PRESSURE1 , 1973 .

[78]  F. James Rohlf,et al.  Biometry: The Principles and Practice of Statistics in Biological Research , 1969 .