Abstract
While ocean acidification is likely to have major effects on many marine organisms, those species that regularly experience variable pCO2 environments may be more tolerant of future predicted changes in ocean chemistry. Euphausia pacifica is an abundant krill species along the Pacific coast of North America and one that regularly experiences varying pCO2 levels during seasonal upwelling, as well as during daily vertical migrations to depth where pCO2 is higher. Krill were collected from Monterey Bay, California (36.8°N, 121.9°W), and experiments were performed from June to August 2014 and maintained at two pCO2 levels (400 and 1200 µatm). Three metabolic responses (oxygen consumption, ingestion rate, and nutrient excretion rates) of E. pacifica were measured. Oxygen consumption declined by 31 % in the first 24 h following exposure to high pCO2 and remained low after 21 days. Oxygen consumption at low pCO2 was low for the first 12 h, increased by 34 % at 24 h, but returned to initial values by 21 days. After 3 weeks of continuous exposure, oxygen consumption rates were 32 % lower in the high pCO2 group. Ingestion and ammonium excretion rates were both significantly lower in the high pCO2 group after 24-h exposure, but not after 7 or 21 days. There was no effect of pCO2 on phosphate excretion. Taken together, these results indicate that E. pacifica has a lower metabolic rate during both short-term (24 h) and longer-term (21 days) exposure to high pCO2. Such metabolic depression may explain previously reported declines in growth of E. pacifica exposed to high pCO2.
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References
Bollens SM, Frost BW, Lin TS (1992) Recruitment, growth, and diel vertical migration of Euphausia pacifica in a temperate fjord. Mar Biol 114(2):219–228. doi:10.1007/BF00349522
Brewer PG, Peltzer ET (2009) Limits to marine life. Science 324(5925):347–348. doi:10.1126/science.1170756
Brinton E (1962) The distribution of Pacific euphausiids. Bulletin of the Scripps Institution of Oceanography, University of California 8:41–270
Brinton E (1976) Population biology of Euphausia pacifica off Southern California. Fish Bull 74(4):733–762
Caldeira K, Wickett ME (2003) Oceanography: anthropogenic carbon and ocean pH. Nature 425(6956):365. doi:10.1038/425365a
Caldeira K, Wickett ME (2005) Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. J Geophys Res 110(C9):C09S04. doi:10.1029/2004JC002671
Calosi P, Rastrick SP, Lombardi C, de Guzman HJ, Davidson L, Jahnke M, Giangrande A, Hardege JD, Schulze A, Spicer JI, Gambi MC (2013) Adaptation and acclimatization to ocean acidification in marine ectotherms: an in situ transplant experiment with polychaetes at a shallow CO2 vent system. Philos Trans R Soc Lond B Biol Sci 368(1627):20120444. doi:10.1098/rstb.2012.0444
Cameron JN, Iwama GK (1987) Compensation of progressive hypercapnia in channel catfish and blue crabs. J Exp Biol 133(1):183–197
Cameron JN, Wood CM (1985) Apparent H+ excretion and CO2 dynamics accompanying carapace mineralization in the blue crab (Callinectes sapidus) following moulting. J Exp Biol 114(1):181–196
Carter HA, Ceballos-Osuna L, Miller NA, Stillman JH (2013) Impact of ocean acidification on metabolism and energetics during early life stages of the intertidal porcelain crab Petrolisthes cinctipes. J Exp Biol 216(Pt 8):1412–1422. doi:10.1242/jeb.078162
Conover RJ (1978) Transformation of organic matter. Marine ecology. Wiley, Chichester, pp 221–499
Cooper H, Potts D, Paytan A (2016) Effects of elevated pCO2 on the survival, growth, and moulting of the Pacific krill species Euphausia pacifica. ICES J Mar Sci. doi:10.1093/icesjms/fsw021
Cripps G, Lindeque P, Flynn KJ (2014) Have we been underestimating the effects of ocean acidification in zooplankton? Glob Chang Biol 20(11):3377–3385. doi:10.1111/gcb.12582
Deigweiher K, Hirse T, Bock C, Lucassen M, Pörtner HO (2010) Hypercapnia induced shifts in gill energy budgets of Antarctic notothenioids. J Comp Physiol B 180(3):347–359. doi:10.1007/s00360-009-0413-x
Diaz RJ, Rosenberg R (2008) Spreading dead zones and consequences for marine ecosystems. Science 321(5891):926–929. doi:10.1126/science.1156401
Dickson AG, Millero FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep Sea Res 34:1733–1743. doi:10.1016/0198-0149(87)90021-5
Dissanayake A, Ishimatsu A (2011) Synergistic effects of elevated CO2 and temperature on the metabolic scope and activity in a shallow-water coastal decapod (Metapenaeus joyneri; Crustacea: penaeidae). ICES J Mar Sci 68(6):1147–1154. doi:10.1093/icesjms/fsq188
Doney SC, Schimel DS (2007) Carbon and climate system coupling on timescales from the precambrian to the anthropocene. Annu Rev Environ Resour 32:31–66. doi:10.1146/annurev.energy.32.041706.124700
Doney SC, Fabry VJ, Feely RA, Kleypas JA (2009) Ocean acidification: the other CO2 problem. Ann Rev Mar Sci 1:169–192. doi:10.1146/annurev.marine.010908.163834
Dupont S, Havenhand J, Thorndyke W, Peck L, Thorndyke M (2008) Near-future level of CO2-driven ocean acidification radically affects larval survival and development in the brittlestar Ophiothrix fragilis. Mar Ecol Prog Ser 373:285–294. doi:10.3354/meps07800
Edenhofer O, Pichs-Madruga R, Sokona Y, Farahani E, Kadner S, Seyboth K (2014) IPCC, 2014: Summary for Policymakers. In: 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 and New York
Enright JT (1977) Diurnal vertical migration: adaptive significance and timing. Part 1. Selective advantage: A metabolic model1. Limnol Oceanogr 22(5):856–872. doi:10.4319/lo.1977.22.5.0856
Fabry VJ, Seibel BA, Feely RA, Orr JC (2008) Impacts of ocean acidification on marine fauna and ecosystem processes. ICES J Mar Sci 65(3):414–432. doi:10.1029/2001GB1459
Feely RA, Sabine CL, Hernandez-Ayon JM, Ianson D, Hales B (2008) Evidence for upwelling of corrosive “acidified” water onto the continental shelf. Science 320(5882):1490–1492. doi:10.1126/science.1155676
Feely RA, Doney SC, Cooley SR (2009) Ocean acidification: present conditions and future changes in a high-CO2 world. Oceanography 22(4):36–47. doi:10.5670/oceanog.2009.95
Gómez-Gutiérrez J, Feinberg LR, Shaw T, Peterson WT (2006) Variability in brood size and female length of Euphausia pacifica among three populations in the North Pacific. Mar Ecol Prog Ser 323:185–194. doi:10.3354/meps323185
Guppy M, Withers P (1999) Metabolic depression in animals: physiological perspectives and biochemical generalizations. Biol Rev Camb Philos Soc 74(1):1–40. doi:10.1017/S0006323198005258
Harris R, Wiebe P, Lenz J, Skjoldal H-R, Huntley M (2000) ICES zooplankton methodology manual. Academic Press, San Diego
Heisler N (1986) Acid-base regulation in animals. Elsevier Science, Michigan
Henry RP, Wheatly MG (1992) Interaction of respiration, ion regulation, and acid-base balance in the everyday life of aquatic crustaceans. Am Zool 32(3):407–416. doi:10.1093/icb/32.3.407
Hildebrandt N, Sartoris FJ, Schulz KG, Riebesell U, Niehoff B (2015) Ocean acidification does not alter grazing in the calanoid copepods Calanus finmarchicus and Calanus glacialis. ICES Journal of Marine Science: Journal du Conseil :fsv226. doi:10.1093/icesjms/fsv226
Holcomb M, McCorkle DC, Cohen AL (2010) Long-term effects of nutrient and CO2 enrichment on the temperate coral Astrangia poculata (Ellis and Solander, 1786). J Exp Mar Biol Ecol 386(1):27–33. doi:10.1016/j.jembe.2010.02.007
Hu MY, Casties I, Stumpp M, Ortega-Martinez O, Dupont S (2014) Energy metabolism and regeneration are impaired by seawater acidification in the infaunal brittlestar Amphiura filiformis. J Exp Biol 217(Pt 13):2411–2421. doi:10.1242/jeb.100024
Isari S, Zervoudaki S, Saiz E, Pelejero C, Peters J (2015) Copepod vital rates under CO2 -induced acidification: a calanoid species and a cyclopoid species under short-term exposures. J Plankton Res 37(5):912–922. doi:10.1093/plankt/fbv057
Kawaguchi S, Kurihara H, King R, Hale L, Berli T, Robinson JP, Ishida A, Wakita M, Virtue P, Nicol S, Ishimatsu A (2011) Will krill fare well under Southern Ocean acidification? Biol Lett 7:288–291. doi:10.1098/rsbl.2010.0777
Kawaguchi S, Ishida A, King R, Raymond B, Waller N, Constable A, Nicol S, Wakita M, Ishimatsu A (2013) Risk maps for Antarctic krill under projected Southern Ocean acidification. Nat Clim Change 3(9):843–847. doi:10.1038/nclimate1937
Kleypas JA, Feely RA, Fabry VJ, Langdon C, Sabine CL, Robbins LL (2006) Impacts of ocean acidification on coral reefs and other marine calcifiers: a guide for future research. Rep of a workshop sponsored by NSF, NOAA & USGS, St. Petersburg, FL, 18–20 April 2005, p 88
Kroeker KJ, Kordas RL, Crim RN, Singh GG (2010) Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol Lett 13(11):1419–1434. doi:10.1111/j.1461-0248.2010.01518.x
Kroeker KJ, Kordas RL, Crim R, Hendriks IE, Ramajo L, Singh GS, Duarte CM, Gattuso J-P (2013) Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob Chang Biol 19(6):1884–1896. doi:10.1111/gcb.12179
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
Kurihara H, Kato S, Ishimatsu A (2007) Effects of increased seawater pCO2 on early development of the oyster Crassostrea gigas. Aquat Biol 1:91–98. doi:10.3354/ab00009
Langenbuch M, Pörtner H-O (2002) Changes in metabolic rate and N excretion in the marine invertebrate Sipunculus nudus under conditions of environmental hypercapnia: identifying effective acid-base variables. J Exp Biol 205(8):1153–1160
Langenbuch M, Pörtner H-O (2004) High sensitivity to chronically elevated CO2 levels in a eurybathic marine sipunculid. Aquat Toxicol 70(1):55–61
Lehman JT (1980) Release and cycling of nutrients between planktonic algae and herbivores. Limnol Oceanogr 25(4):620–632. doi:10.4319/lo.1980.25.4.0620
Lewis CN, Brown KA, Edwards LA, Cooper G, Findlay HS (2013) Sensitivity to ocean acidification parallels natural pCO2 gradients experienced by Arctic copepods under winter sea ice. Proc Natl Acad Sci USA 110(51):E4960–E4967. doi:10.1073/pnas.1315162110
Li W, Gao K (2012) A marine secondary producer respires and feeds more in a high CO2 ocean. Mar Pollut Bull 64(4):699–703. doi:10.1016/j.marpolbul.2012.01.033
Li W, Han G, Dong Y, Ishimatsu A, Russell BD, Gao K (2015) Combined effects of short-term ocean acidification and heat shock in a benthic copepod Tigriopus japonicus Mori. Mar Biol 162(9):1901–1912
Maas AE, Wishner KF, Seibel BA (2012) The metabolic response of pteropods to acidification reflects natural CO2-exposure in oxygen minimum zones. Biogeosciences 9:747–757. doi:10.5194/bg-9-747-2012
Marinovic B, Mangel M (1999) Krill can shrink as an ecological adaptation to temporarily unfavorable environments. Ecol Lett 2:338–343
Mehrbach C, Culberson CH, Hawley JE, Pytkowicz RM (1973) Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol Oceanogr 18:897–907
Melzner F, Gutowska MA, Langenbuch M, Dupont S, Lucassen M, Thorndyke MC, Bleich M, Pörtner HO (2009) Physiological basis for high CO2 tolerance in marine ectothermic animals: pre-adaptation through lifestyle and ontogeny? Biogeosciences 6:2313–2331. doi:10.5194/bg-6-2313-2009
Miles H, Widdicombe S, Spicer JI, Hall-Spencer J (2007) Effects of anthropogenic seawater acidification on acid–base balance in the sea urchin Psammechinus miliaris. Mar Pollut Bull 54(1):89–96. doi:10.1016/j.marpolbul.2006.09.021
Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, Feely RA, Gnanadesikan A, Gruber N, Ishida A, Joos F (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437(7059):681–686. doi:10.1038/nature04095
Pane EF, Barry JP (2007) Extracellular acid-base regulation during short-term hypercapnia is effective in a shallow-water crab, but ineffective in a deep-sea crab. Mar Ecol Prog Ser 334:1–9. doi:10.3354/meps334001
Pespeni MH, Chan F, Menge BA, Palumbi SR (2013) Signs of adaptation to local pH conditions across an environmental mosaic in the California Current Ecosystem. Integr Comp Biol 53(5):857–870. doi:10.1093/icb/ict094
Pierrot D, Lewis E, Wallace D.W.R. (2006) MS excel program developed for CO2 system calculations [computer file]. ORNL/CDIAC-105a Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, US Department of Energy [distributor]
Pörtner HO, Langenbuch M, Reipschläger A (2004) Biological impact of elevated ocean CO2 concentrations: lessons from animal physiology and earth history. J Oceanogr 60(4):705–718. doi:10.1007/s10872-004-5763-0
Pörtner HO, Langenbuch M, Michaelidis B (2005) Synergistic effects of temperature extremes, hypoxia, and increases in CO2 on marine animals: From Earth history to global change. J Geophys Res 110(C9):C09S10. doi:10.1029/2004JC002561
Roman MR, Rublee PA (1980) Containment effects in copepod grazing experiments: a plea to end the black box approach. Limnol Oceanogr 25(6):982–990. doi:10.4319/lo.1980.25.6.0982
Rosa R, Seibel BA (2008) Synergistic effects of climate-related variables suggest future physiological impairment in a top oceanic predator. Proc Natl Acad Sci USA 105(52):20776–20780. doi:10.1073/pnas.0806886105
Ross PM, Parker L, O’Connor WA, Bailey EA (2011) The impact of ocean acidification on reproduction, early development and settlement of marine organisms. Water 3(4):1005–1030. doi:10.3390/w3041005
Saba GK, Schofield O, Torres JJ, Ombres EH, Steinberg DK (2012) Increased feeding and nutrient excretion of adult Antarctic krill, Euphausia superba, exposed to enhanced carbon dioxide (CO2). PLoS ONE 7(12):e52224. doi:10.1371/journal.pone.0052224
Seibel BA (2003) Biological impacts of deep-sea carbon dioxide injection inferred from indices of physiological performance. J Exp Biol 206(4):641–650. doi:10.1242/jeb.00141
Seibel BA (2011) Critical oxygen levels and metabolic suppression in oceanic oxygen minimum zones. J Exp Biol 214(Pt 2):326–336. doi:10.1242/jeb.049171
Solomon S (2007) Climate Change 2007: the physical science basis: contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge and New York
Stocker TF, Qin Q, Plattner G-K, et al. (2013) Summary for Policymakers. In: 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 University Press, Cambridge and New York
Stramma L, Johnson GC, Sprintall J, Mohrholz V (2008) Expanding oxygen-minimum zones in the tropical oceans. Science 320(5876):655–658. doi:10.1126/science.1153847
Stumpp M, Trübenbach K, Brennecke D, Hu MY, Melzner F (2012) Resource allocation and extracellular acid-base status in the sea urchin Strongylocentrotus droebachiensis in response to CO2 induced seawater acidification. Aquat Toxicol 110–111:194–207. doi:10.1016/j.aquatox.2011.12.020
Takahashi M, Ikeda T (1975) Excretion of ammonia and inorganic phosphorus by Euphausia pacifica and Metridia pacifica at different concentrations of phytoplankton. J Fish Res Bd Can 32(11):2189–2195. doi:10.1139/f75-257
Thomsen J, Melzner F (2010) Moderate seawater acidification does not elicit long-term metabolic depression in the blue mussel Mytilus edulis. Mar Biol 157(12):2667–2676. doi:10.1139/f75-257
Thor P, Dupont S (2015) Transgenerational effects alleviate severe fecundity loss during ocean acidification in a ubiquitous planktonic copepod. Glob Chang Biol 21(6):2261–2271
Tremblay N (2014) Tolerance mechanisms and responses of krill species of different latitudes to oxygen minimum zones. Dissertation, Universität Bremen, Bremen, Germany
Vaulot D, Chisholm SW (1987) A simple model of the growth of phytoplankton populations in light/dark cycles. J Plankton Res 9(2):345–366. doi:10.1093/plankt/9.2.345
Wheatly MG, Henry RP (1992) Extracellular and intracellular acid-base regulation in crustaceans. J Exp Zool 263(2):127–142. doi:10.1002/jez.1402630204
Whiteley NM (2011) Physiological and ecological responses of crustaceans to ocean acidification. Mar Ecol Prog Ser 430:257–271. doi:10.3354/meps09185
Whiteley NM, Scott JL, Breeze SJ, McCann L (2001) Effects of water salinity on acid-base balance in decapod crustaceans. J Exp Biol 204(5):1003–1011
Widdicombe S, Spicer JI (2008) Predicting the impact of ocean acidification on benthic biodiversity: what can animal physiology tell us? J Exp Mar Biol Ecol 366(1):187–197. doi:10.1016/j.jembe.2008.07.024
Wood HL, Spicer JI, Widdicombe S (2008) Ocean acidification may increase calcification rates, but at a cost. Proc R Soc 275(1644):1767–1773. doi:10.1098/rspb.2008.0343
Zervoudaki S, Frangoulis C, Giannoudi L, Krasakopoulou E (2013) Effects of low pH and raised temperature on egg production, hatching and metabolic rates of a Mediterranean copepod species (Acartia clausi) under oligotrophic conditions. Medit Mar Sci. doi:10.12681/mms.553
Acknowledgments
The authors would like to thank Luis Hernandez, Honor Weber, and Sarah Dondelinger for laboratory help and assistance with water chemistry analyses; Dave Benet and Steve Clabuesch for assistance in building the pCO2-air mixing system and with krill collections; Betsy Steele for culturing phytoplankton and general laboratory guidance; and Rob Franks for assistance with nutrient and chemical analyses.
Funding
This study was funded through awards from the NOAA West Coast and Polar Regions Undersea Research Center (project FP12783A) and NSF (OCE-1040952) to A. Paytan, a UCSC Committee on Research grant and a gift from the Mitsubishi corporation to D. Potts, and awards to H. Cooper from the Friends of Long Marine Laboratory, Meyers Trust, and the UCSC 503 Department of Ecology and Evolutionary Biology.
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Cooper, H.L., Potts, D.C. & Paytan, A. Metabolic responses of the North Pacific krill, Euphausia pacifica, to short- and long-term pCO2 exposure. Mar Biol 163, 207 (2016). https://doi.org/10.1007/s00227-016-2982-z
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DOI: https://doi.org/10.1007/s00227-016-2982-z