Abstract
Researchers have investigated the immediate effects of end-of-century climate change scenarios on many marine species, yet it remains unclear whether we can reliably predict how marine species may respond to future conditions because biota may become either more or less resistant over time. Here, we examined the role of pre-exposure to elevated temperature and reduced pH in mitigating the potential negative effects of future ocean conditions on polyps of a dangerous Irukandji jellyfish Alatina alata. We pre-exposed polyps to elevated temperature (28 °C) and reduced pH (7.6), in a full factorial experiment that ran for 14 d. We secondarily exposed original polyps and their daughter polyps to either current (pH 8.0, 25 °C) or future conditions (pH 7.6, 28 °C) for a further 34 d to assess potential phenotypic plastic responses and whether asexual offspring could benefit from parental pre-exposure. Polyp fitness was characterised as asexual reproduction, respiration, feeding, and protein concentrations. Pre-exposure to elevated temperature alone partially mitigated the negative effects of future conditions on polyp fitness, while pre-exposure to reduced pH in isolation completely mitigated the negative effects of future conditions on polyp fitness. Pre-exposure to the dual stressors, however, reduced fitness under future conditions relative to those in the control treatment. Under future conditions, polyps had higher respiration rates regardless of the conditions they were pre-exposed to, suggesting that metabolic rates will be higher under future conditions. Parent and daughter polyps responded similarly to the various treatments tested, demonstrating that parental pre-exposure did not confer any benefit to asexual offspring under future conditions. Importantly, we demonstrate that while pre-exposure to the stressors individually may allow Irukandji polyps to acclimate over short timescales, the stressors are unlikely to occur in isolation in the long term, and thus, warming and acidification in parallel may prevent polyp populations from acclimating to future ocean conditions.
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07 June 2017
An erratum to this article has been published.
References
Bay RA, Palumbi SR (2015) Rapid acclimation ability mediated by transcriptome changes in reef-building corals. Genome Biol Evol 7:1602–1612
Bell G (2013) Evolutionary rescue and the limits of adaptation. Philos Trans R Soc Lond B Biol Sci 368:20120080
Bellantuono AJ, Hoegh-Guldberg O, Rodriguez-Lanetty M (2011) Resistance to thermal stress in corals without changes in symbiont composition. Proc R Soc Lond B Biol Sci 279:1100–1107
Bockmon E, Frieder C, Navarro M, White-Kershek L, Dickson A (2013) Controlled experimental aquarium system for multi-stressor investigation of carbonate chemistry, oxygen saturation, and temperature. Biogeosciences 10:5967–5975
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
Calow P (1991) Physiological costs of combating chemical toxicants: ecological implications. Comp Biochem Physiol C Comp Pharmacol 100:3–6
Carrette TJ, Underwood AH, Seymour JE (2012) Irukandji syndrome: a widely misunderstood and poorly researched tropical marine envenoming. Diving Hyperb Med 42:214–223
Carrette TJ, Straehler-Pohl I, Seymour J (2014) Early life history of Alatina cf. moseri populations from Australia and Hawaii with implications for taxonomy (Cubozoa: Carybdeida, Alatinidae). PLoS One 9:e84377
Chivers WJ, Walne AW, Hays GC (2017) Mismatch between marine plankton range movements and the velocity of climate change. Nat Commun 8:14434
Courtney R, Seymour J (2013) Seasonality in polyps of a tropical cubozoan: Alatina nr mordens. PLoS One 8:e69369
Dickson AG, Sabine CL, Christian JR (2007) Guide to best practices for ocean CO2 measurements. PICES Special Publication 3, North Pacific Marine Science Organization, Sidney, BC, Canada, 191 pp
Donelson J, Munday P, McCormick M, Pitcher C (2012) Rapid transgenerational acclimation of a tropical reef fish to climate change. Nat Clim Chang 2:30–32
Dupont S, Dorey N, Stumpp M, Melzner F, Thorndyke M (2013) Long-term and trans-life-cycle effects of exposure to ocean acidification in the green sea urchin Strongylocentrotus droebachiensis. Mar Biol 160:1835–1843
Foo SA, Byrne M (2016) Acclimatization and adaptive capacity of marine species in a changing ocean. Adv Mar Biol 74:69–116
Form AU, Riebesell U (2012) Acclimation to ocean acidification during long-term CO2 exposure in the cold-water coral Lophelia pertusa. Glob Chang Biol 18:843–853
Frieder CA, Gonzalez JP, Bockmon EE, Navarro MO, Levin LA (2014) Can variable pH and low oxygen moderate ocean acidification outcomes for mussel larvae? Glob Chang Biol 20:754–764
Gershwin LA, De Nardi M, Winkel KD, Fenner PJ (2010) Marine stingers: review of an under-recognized global coastal management issue. Coast Manage 38:22–41
Gershwin LA, Condie SA, Mansbridge JV, Richardson AJ (2014) Dangerous jellyfish blooms are predictable. J R Soc Interface 11:20131168
Gibbin EM, Putnam HM, Davy SK, Gates RD (2014) Intracellular pH and its response to CO2-driven seawater acidification in symbiotic versus non-symbiotic coral cells. J Exp Biol 217:1963–1969
Grady JD, Burnett JW (2003) Irukandji-like syndrome in South Florida divers. Ann Emerg Med 42:763–766
Harvey BP, Gwynn-Jones D, Moore PJ (2013) Meta-analysis reveals complex marine biological responses to the interactive effects of ocean acidification and warming. Ecol Evol 3:1016–1030
Hettinger A, Sanford E, Hill TM, Russell AD, Sato KN, Hoey J, Forsch M, Page HN, Gaylord B (2012) Persistent carry-over effects of planktonic exposure to ocean acidification in the Olympia oyster. Ecology 93:2758–2768
Hofmann GE, Smith JE, Johnson KS, Send U, Levin LA, Micheli F, Paytan A, Price NN, Peterson B, Takeshita Y (2011) High-frequency dynamics of ocean pH: a multi-ecosystem comparison. PLoS One 6:e28983
IPCC (2014) Climate change 2014: synthesis report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. IPCC, Geneva, Switzerland
Klein SG, Pitt KA, Rathjen KA, Seymour JE (2014) Irukandji jellyfish polyps exhibit tolerance to interacting climate change stressors. Glob Chang Biol 20:28–37
Klein SG, Pitt KA, Nitschke MR, Goyen S, Welsh DT, Suggett DJ, Carroll AR (2017) Symbiodinium mitigate the combined effects of hypoxia and acidification on a non-calclifying cnidarian. Glob Chang Biol. doi:10.1111/gcb.13718
Kroeker KJ, Kordas RL, Crim R, Hendriks IE, Ramajo L, Singh GS, Duarte CM, Gattuso J (2013) Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob Chang Biol 19:1884–1896
Laurent J, Tambutté S, Tambutté É, Allemand D, Venn A (2013) The influence of photosynthesis on host intracellular pH in scleractinian corals. J Exp Biol 216:1398–1404
Laurent J, Venn A, Tambutté É, Ganot P, Allemand D, Tambutté S (2014) Regulation of intracellular pH in cnidarians: response to acidosis in Anemonia viridis. FEBS J 281:683–695
Lawley JW, Ames CL, Bentlage B, Yanagihara A, Goodwill R, Kayal E, Hurwitz K, Collins AG (2016) Box jellyfish Alatina alata has a circumtropical distribution. Biol Bull 231:152–169
Lemoine NP, Burkepile DE (2012) Temperature-induced mismatches between consumption and metabolism reduce consumer fitness. Ecology 93:2483–2489
Lewis E, Wallace D, Allison LJ (1998) Program developed for CO2 system calculations. ORNL/CDIAC-105, Carbon Dioxide Information Analysis Center, US Department of Energy, TN
Logan CA, Dunne JP, Eakin CM, Donner SD (2014) Incorporating adaptive responses into future projections of coral bleaching. Glob Chang Biol 20:125–139
Michaelidis B, Ouzounis C, Paleras A, Pörtner HO (2005) Effects of long-term moderate hypercapnia on acid–base balance and growth rate in marine mussels. Mytilus galloprovincialis. Mar Ecol Prog Ser 293:109–118
Middlebrook R, Hoegh-Guldberg O, Leggat W (2008) The effect of thermal history on the susceptibility of reef-building corals to thermal stress. J Exp Biol 211:1050–1056
Miller GM, Watson S-A, Donelson JM, McCormick MI, Munday PL (2012) Parental environment mediates impacts of increased carbon dioxide on a coral reef fish. Nat Clim Chang 2:858–861
Moya A, Huisman L, Ball E, Hayward D, Grasso L, Chua C, Woo H, Gattuso JP, Foret S, Miller DJ (2012) Whole transcriptome analysis of the coral Acropora millepora reveals complex responses to CO2-driven acidification during the initiation of calcification. Mol Ecol 21:2440–2454
Munday PL (2014) Transgenerational acclimation of fishes to climate change and ocean acidification. F1000Prime Rep 6:99
Munday PL, Warner RR, Monro K, Pandolfi JM, Marshall DJ (2013) Predicting evolutionary responses to climate change in the sea. Ecol Lett 16:1488–1500
Nagelkerken I, Munday PL (2015) Animal behaviour shapes the ecological effects of ocean acidification and warming: moving from individual to community-level responses. Glob Chang Biol 22:974–989
Nagelkerken I, Pitt KA, Rutte MD, Geertsma RC (2016) Ocean acidification alters fish–jellyfish symbiosis. Proc R Soc Lond B Biol Sci 283:20161146
Oliver T, Palumbi S (2011) Do fluctuating temperature environments elevate coral thermal tolerance? Coral Reefs 30:429–440
Parker LM, O’Connor WA, Raftos DA, Pörtner HO, Ross PM (2015) Persistence of positive carryover effects in the oyster Saccostrea glomerata, following transgenerational exposure to ocean acidification. PLoS One 10:e0132276
Pennington JT, Chavez FP (2000) Seasonal fluctuations of temperature, salinity, nitrate, chlorophyll and primary production at station H3/M1 over 1989–1996 in Monterey Bay, California. Deep Sea Res Part 2 Top Stud Oceanogr 47:947–973
Pespeni MH, Sanford E, Gaylord B, Hill TM, Hosfelt JD, Jaris HK, LaVigne M, Lenz EA, Russell AD, Young MK (2013) Evolutionary change during experimental ocean acidification. Proc Natl Acad Sci U S A 110:6937–6942
Pommier P, Coulange M, De Haro L (2005) Systemic envenomation by jellyfish in Guadeloupe: Irukandji-like syndrome? Med Trop (Mars) 65:367–369
Pörtner H (2008) Ecosystem effects of ocean acidification in times of ocean warming: a physiologist’s view. Mar Ecol Prog Ser 373:203–217
Pörtner HO, Bock C (2000) A contribution of acid–base regulation to metabolic depression in marine ectotherms. In: Heldmaier G, Klingenspor M (eds) Life in the cold. Springer, Berlin Heidelberg, pp 443–458
Pörtner HO, Peck LS, Hirse T (2006) Hyperoxia alleviates thermal stress in the Antarctic bivalve, Laternula elliptica: evidence for oxygen limited thermal tolerance. Polar Biol 29:688–693
Putnam HM, Gates RD (2015) Preconditioning in the reef-building coral Pocillopora damicornis and the potential for trans-generational acclimatization in coral larvae under future climate change conditions. J Exp Biol 218:2365–2372
Reipschläger A, Pörtner H-O (1996) Metabolic depression during environmental stress: the role of extracellular versus intracellular pH in Sipunculus nudus. J Exp Biol 199:1801–1807
Sokolova IM (2013) Energy-limited tolerance to stress as a conceptual framework to integrate the effects of multiple stressors. Integr Comp Biol 2013:ict028
Suckling CC, Clark MS, Beveridge C, Brunner L, Hughes AD, Harper EM, Cook EJ, Davies AJ, Peck LS (2014) Experimental influence of pH on the early lifestages of sea urchins II: increasing parental exposure times gives rise to different responses. Invertebr Reprod Dev 58:161–175
Sunday JM, Calosi P, Dupont S, Munday PL, Stillman JH, Reusch TB (2014) Evolution in an acidifying ocean. Trends Ecol Evol 29:117–125
Thor P, Dupont S (2015) Transgenerational effects alleviate severe fecundity loss during ocean acidification in a ubiquitous planktonic copepod. Glob Chang Biol 21:2261–2271
Towle EK, Baker AC, Langdon C (2016) Preconditioning to high CO2 exacerbates the response of the Caribbean branching coral Porites porites to high temperature stress. Mar Ecol Prog Ser 546:75–84
van Oppen MJ, Oliver JK, Putnam HM, Gates RD (2015) Building coral reef resilience through assisted evolution. Proc Natl Acad Sci U S A 112:2307–2313
Verhoeven KJ, Jansen JJ, Van Dijk PJ, Biere A (2010) Stress-induced DNA methylation changes and their heritability in asexual dandelions. New Phytol 185:1108–1118
Wood HL, Spicer JI, Widdicombe S (2008) Ocean acidification may increase calcification rates, but at a cost. Proc R Soc Lond B Biol Sci 275:1767–1773
Yoshimoto CM, Yanagihara AA (2002) Cnidarian (coelenterate) envenomations in Hawai’i improve following heat application. Trans R Soc Trop Med Hyg 96:300–303
Acknowledgements
Funding for this study was provided by Griffith University and an Australian Postgraduate Award to S.G.K. We thank W. Bennett, F. Leusch, D. Welsh, and D. Tonzing for technical assistance and J. Arthur and J. Hay for statistical advice. We also thank R. Courtney and J. Seymour from James Cook University, Townsville, for cultures of A. alata polyps.
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Communicated by Biology Editor Dr. Line K. Bay
An erratum to this article is available at https://doi.org/10.1007/s00338-017-1599-0.
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Klein, S.G., Pitt, K.A. & Carroll, A.R. Pre-exposure to simultaneous, but not individual, climate change stressors limits acclimation capacity of Irukandji jellyfish polyps to predicted climate scenarios. Coral Reefs 36, 987–1000 (2017). https://doi.org/10.1007/s00338-017-1590-9
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DOI: https://doi.org/10.1007/s00338-017-1590-9