Skip to main content

Advertisement

SpringerLink
Log in

Elevated temperature elicits greater effects than decreased pH on the development, feeding and metabolism of northern shrimp (Pandalus borealis) larvae

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Climate models predict that the average temperature in the North Sea could increase 3–5 °C and surface-waters pH could decrease 0.3–0.5 pH units by the end of this century. Consequently, we investigated the combined effect of decreased pH (control pH 8.1; decreased pH 7.6) and temperature (control 6.7 °C; elevated 9.5 °C) on the hatching timing and success, and the zoeal development, survival, feeding, respiration and growth (up to stage IV zoea) of the northern shrimp, Pandalus borealis. At elevated temperature, embryos hatched 3 days earlier, but experienced 2–4 % reduced survival. Larvae developed 9 days faster until stage IV zoea under elevated temperature and exhibited an increase in metabolic rates (ca 20 %) and an increase in feeding rates (ca 15–20 %). Decreased pH increased the development time, but only at the low temperature. We conclude that warming will likely exert a greater effect on shrimp larval development than ocean acidification manifesting itself as accelerated developmental rates with greater maintenance costs and decreased recruitment in terms of number and size.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Allen JA (1959) On the biology of Pandalus borealis Krøyer, with reference to a population off the Northumberland coast. J Mar Biol Assoc UK 38:189–220

    Article  Google Scholar 

  • Ariza P, Ouellet P (2009) Diet components of northern shrimp Pandalus borealis first stage larvae in the Northwest Gulf of St. Lawrence. J Crust Biol 29:532–543

    Article  Google Scholar 

  • Arnold KE, Findlay HS, Spicer JI, Daniels CL, Boothroyd D (2009) Effect of CO2-related acidification on aspects of the larval development of the European lobster, Homarus gammarus (L.). Biogeosciences 6:1747–1754

    Article  CAS  Google Scholar 

  • Aschan M, Ingvaldsen R (2009) Recruitment of shrimp (Pandalus borealis) in the Barents Sea related to spawning stock and environment. Deep Sea Res Part II 56:2012–2022

    Article  Google Scholar 

  • Bechmann RK, Taban IC, Westerlund S, Godal BF, Arnberg M, Vingen S, Ingvarsdottir A, Baussant T (2010) Effects of ocean acidification on early life stages of shrimp (Pandalus borealis) and mussel (Mytilus edulis). J Toxicol Environ Health Part A 74:424–438

    Article  Google Scholar 

  • Bellerby RGJ, Schulz KG, Riebesell U, Neill C, Nondal G, Heegaard E, Johannessen T, Brown KR (2008) Marine ecosystem community carbon and nutrient uptake stoichiometry under varying ocean acidification during the PeECE III experiment. Biogeosciences 5:1517–1527

    Article  CAS  Google Scholar 

  • Bergström BI (2000) The biology of Pandalus. Adv Mar Biol 38:55–245

    Article  Google Scholar 

  • Brillon S, Lambert Y, Dodson J (2005) Egg survival, embryonic development, and larval characteristics of northern shrimp (Pandalus borealis) females subject to different temperature and feeding conditions. Mar Biol 147:895–911

    Article  Google Scholar 

  • Butler TH (1964) Growth, reproduction, and distribution of Pandalid shrimps in British Columbia. J Fish Res Board Can 21:1403–1452

    Article  Google Scholar 

  • Byrne M (2011) Impact of ocean warming and ocean acidification on marine invertebrate life history stages: vulnerabilities and potential for persistence in a changing ocean. Ocean Mar Biol Ann Rev 49:1–42

    Google Scholar 

  • Byrne M (2012) Global change ecotoxicology: identification of early life history bottlenecks in marine invertebrates, variable species responses and variable experimental approaches. Mar Environ Res 76:3–15

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Caldeira K, Wickett ME (2005) Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. J Geophys Res 110:C09S04

    Article  Google Scholar 

  • Chabot D, Ouellet P (2005) Rearing Pandalus borealis larvae in the laboratory. Mar Biol 147:881–894

    Article  Google Scholar 

  • Chen IC, Hill JK, Ohlemüller R, Roy DB, Thomas CD (2011) Rapid range shifts of species associated with high levels of climate warming. Science 6045:1024–1026

    Article  Google Scholar 

  • Clarke A, Gore DJ (1992) Egg size and composition in Ceratoserolis (Crustacea: Isopoda) from the Weddell Sea. Polar Biol 12:129–134

    Article  Google Scholar 

  • Collins S, Bell G (2004) Phenotypic consequences of 1,000 generations of selection at elevated CO2 in a green alga. Nature 431:566–569

    Article  CAS  Google Scholar 

  • Collins S, Bell G (2006) Evolution of natural algal populations at elevated CO2. Ecol Lett 9:129–135

    Article  Google Scholar 

  • Cossins AR, Bowler K (1987) Temperature biology of animals. Chapman & Hall, London

    Book  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Dickson AG, Millero FJ (1987) A comparison of equilibrium constants for the dissociation of carbonic acid in seawater media. Deep-Sea Res 34:1733–1743

    Article  CAS  Google Scholar 

  • 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 68:1147–1154

    Article  Google Scholar 

  • Doney SC, Balch WC, Fabry VJ, Feely RA (2009) Ocean acidification: a critical emerging problem for the ocean sciences. Oceanography 22:16–25

    Article  Google Scholar 

  • Dupont S, Thorndyke M (2009) Impact of CO2-driven ocean acidification on invertebrates early life-history—what we know, what we need to know and what we can do. Biogeosciences Discuss 6:3109–3131

    Article  Google Scholar 

  • Dupont S, Ortega-Martinez O, Thorndyke M (2010) Impact of near-future ocean acidification on echinoderms. Ecotoxicology 19:449–462

    Article  CAS  Google Scholar 

  • Dupont S, Dorey N, Stumpp M, Melzner F, Thorndyke M (2012) Long-term and trans-life-cycle effects of exposure to ocean acidification in the green sea urchin Strongylocentrotus droebachiensis. Mar Biol. doi:10.1007/s00227-012-1921

    Google Scholar 

  • Findlay HS, Kendall MA, Spicer JI, Turley C, Widdicombe S (2008) Novel microcosm system for investigating the effects of elevated carbon dioxide and temperature on intertidal organisms. Aquat Biol 3:51–62

    Article  Google Scholar 

  • Findlay HS, Kendall MA, Spicer JI, Widdicombe S (2010) Post-larval development of two intertidal barnacles at elevated CO2 and temperature. Mar Biol 157:725–735

    Article  Google Scholar 

  • Findlay HS, Wood HL, Kendall MA, Spicer JI, Twitchett RJ, Widdicombe S (2011a) Comparing the impact of high CO2 on calcium carbonate structures in different marine organisms. Mar Biol Res 7:565–575

    Article  Google Scholar 

  • Findlay HS, Calosi P, Crawfurd K (2011b) Determinants of the PIC: POC response in the coccolithophore Emiliania huxleyi under future ocean acidification scenarios. Limnol Ocean 56:1168–1178

    Article  CAS  Google Scholar 

  • Garcia EG, Sims DW (2007) The northern shrimp (Pandalus borealis) offshore fishery in the Northeast Atlantic. Adv Mar Biol 52:147–266

    Article  Google Scholar 

  • Harvey M, Morrier G (2003) Laboratory feeding experiments on zoea of northern shrimp Pandalus borealis fed with natural zooplankton. Mar Ecol Prog Ser 265:165–174

    Article  Google Scholar 

  • Haynes E (1979) Description of larvae of the northern Shrimp, Pandalus borealis, reared in situ in Kachemak Bay, Alaska. Fish Bull 77:157–173

    Google Scholar 

  • Heming TA (1982) Effects of temperature on utilization of yolk by Chinook Salmon (Oncorhynchus tshawytscha) eggs and alevins. Can J Fish Aquat Sci 39:184–190

    Article  Google Scholar 

  • Jones SJ, Mieszkowska N, Wethey DS (2009) Linking thermal tolerances and biogeography: Mytilus edulis (L.) at its southern limit on the East coast of the United States. Biol Bull 217:73–85

    Google Scholar 

  • Koeller P, Fuentes-Yaco C, Platt T, Sathyendranath S, Richards A, Ouellet P, Orr D, Skuladottir U, Wieland K, Savard L, Aschan M (2009) Basin-scale coherence in phenology of shrimps and phytoplankton in the North Atlantic Ocean. Science 324:791–793

    Article  CAS  Google Scholar 

  • Kroeker KJ, Kordas RL, Crim RN, Singh GG (2010) Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol Lett 13:1419–1434

    Article  Google Scholar 

  • 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 56:1086–1090

    Article  CAS  Google Scholar 

  • Lischka S, Budenbender J, Boxhammer T, Riebesell U (2011) Impact of ocean acidification and elevated temperatures on early juveniles of the polar shelled pteropod Limacina helicina: mortality, shell degradation, and shell growth. Biogeosciences 8:919–932

    Article  CAS  Google Scholar 

  • Lohbeck KT, Riebesell U, Reusch TBH (2012) Adaptive evolution of a key phytoplankton species to ocean acidification. Nat Geosci 5:346–351

    Article  CAS  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 

  • McDonald MR, McClintock JB, Amsler CD, Rittschof D, Angus RA, Orihuela B (2009) Effects of ocean acidification on larval development and settlement of the common intertidal barnacle Amphibalanus amphitrite. Integr Comp Biol 49:E270

    Google Scholar 

  • Mehrbach C, Cullberson CH, Hawley JE, Pytkowicz RM (1973) Measurements of the apparent dissociation constants of carbonic acids in seawater at atmospheric pressure. Limnol Oceanogr 18:897–907

    Article  CAS  Google Scholar 

  • Melatunan S, Calosi P, Rundle SD, Moody J, Widdicombe S (2011) Exposure to elevated temperature and pCO2 reduces respiration rate and energy status in the periwinkle Littorina littorea. Physiol Biochem Zool 84:583–594

    Article  CAS  Google Scholar 

  • Metzger R, Sartoris FJ, Langenbuch M, Pörtner HO (2007) Influence of elevated CO2 concentrations on thermal tolerance of the edible crab Cancer Pagurus. J Therm Biol 3:144–151

    Article  Google Scholar 

  • Mikkelsen A, Engelsen SB, Hansen HCB, Larsen O, Skibsted LH (1997) Calcium carbonate crystallization in the α-chitin matrix of the shell of pink shrimp, Pandalus borealis, during frozen storage. J Cryst Growth 177:125–134

    Article  CAS  Google Scholar 

  • Nunes P, Nishiyama T (1984) Effects of temperature on the embryonic development of the northern pink shrimp Pandalus borealis Krøyer. J Shellfish Res 4:96–97

    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-K, Rodgers KB, Sabine CL, Sarmiento JL, Schlitzer R, Slater RD, Totterdell IJ, Weirig M-F, 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 

  • Ouellet P, Chabot D (2005) Rearing Pandalus borealis; (Krøyer) larvae in the laboratory. Mar Biol 147:869–880

    Article  Google Scholar 

  • Ouellet P, Fuentes-Yaco CS, Savard L, Platt T, Sathyendranath S, Koeller P, Orr D, Siegstad H (2011) Ocean surface characteristics influence recruitment variability of populations of northern shrimp (Pandalus borealis) in the Northwest Atlantic. ICES J Mar Sci 68:737–744

    Article  Google Scholar 

  • Pansch C, Nasrolahi A, Appelhans YS, Wahl M (2012) Impacts of ocean warming and acidification on the larval development of the barnacle Amphibalanus improvisus. J Exp Mar Biol Ecol 420–42:48–55

    Article  Google Scholar 

  • Parker LM, Ross PM, O’Connor WA, Borysko L, Raftos DA, Pörtner HO (2012) Adult exposure influences offspring response to ocean acidification in oysters. Glob Change Biol 18:82–92

    Article  Google Scholar 

  • Paul AJ, Nunes P (1983) Temperature modification of respiratory metabolism and caloric intake of Pandalus borealis (Krøyer) first zoeae. J Exp Mar Biol Ecol 66:163–168

    Article  Google Scholar 

  • Pedersen SA, Storm L (2002) Northern Shrimp (Pandalus borealis) recruitment in West Greenland waters Part II. Lipid classes and fatty acids in Pandalus shrimp larvae: implications for survival expectations and trophic relationships. J Northwest Atl Fish Sci 30:47–60

    Article  Google Scholar 

  • Pierrot D, Lewis DE, Wallace DWR (2006) CO2SYS.EXE—MS excel program developed for CO2 system calculations. ORNL/CDIAC-105a. http://cdiac.ornl.gov/ftp/co2sys/. Oak Ridge, Tennessee. Carbon Dioxide Information Center, Oak Ridge National Laboratory, U.S. Department of Energy

  • Pistevos JCA, Calosi P, Widdicombe S, Bishop JDD (2011) Will variation among genetic individuals influence species responses to global climate change? Oikos 120:675–689

    Article  Google Scholar 

  • Pörtner HO, Farrell AP (2008) Physiology and Climate Change. Science 322:690–692

    Article  Google Scholar 

  • Pörtner HO, Berdal B, Blust R, Brix O, Colosimo A, De Wachter B, Giuliani A, Johansen T, Fischer T, Knust R, Lannig G, Naevdal G, Nedenes A, Nyhammer G, Sartoris FJ, Serendero I, Sirabella P, Thorkildsen S, Zakhartsev M (2001) Climate induced temperature effects on growth performance, fecundity and recruitment in marine fish: developing a hypothesis for cause and effect relationships in Atlantic cod (Gadus morhua) and common eelpout (Zoarces viviparus). Cont Shelf Res 21:1975–1997

    Article  Google Scholar 

  • Ries JB, Cohen AL, McCorkle DC (2009) Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37:1131–1134

    Article  CAS  Google Scholar 

  • 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 105:20776–20780

    Article  CAS  Google Scholar 

  • Schiettecatte LS, Helmuth T, Borges AV, Frankignoulle M (2006) Traditional normalized total alkalinity as a tracer of the surface seawater masses of the North Sea. In: Poster presented at the EGS-AGU-EUG, Joint Assembly. Nice, France, 06–11 April 2003

  • Shumway SE, Perkins HC, Schick DF, Stickney AP (1985) Synopsis of biological data on the pink shrimp, Pandalus borealis (Kroyer). NOAA Technical Report, No NMFS-30: 55 p

  • Sibly RM, Calow P (1986) Physiological ecology of animals: An evolutionary approach. Blackwell Scientific Publications, Oxford

    Google Scholar 

  • Sokal RR, Rolhf FJ (1995) Biometry: the principles and practice of statistics in biological research, 3rd edn. W. H. Freeman

  • Sokolov AP, Stone PH, Forest CE, Prinn R, Sarofim MC, Webster M, Paltsev S, Schlosser CA, Kicklighter D, Dutkiewicz S, Reilly J, Wang C, Felzer B, Melillo JM, Jacoby HD (2009) Probabilistic forecast for twenty-first-century climate based on uncertainties in emissions (without policy) and climate parameters. J Clim 22:5175–5204

    Article  Google Scholar 

  • Southward AJ, Hawkins SJ, Burrows MT (1995) Seventy years’ observations of changes in distribution and abundance of zooplankton and intertidal organisms in the western English Channel in relation to rising sea temperature. J Therm Biol 20:127–155

    Article  Google Scholar 

  • Spicer JI, Gaston K (1999) Physiological diversity and its ecological implications. Blackwells Science, Oxford

    Google Scholar 

  • Stillman JH (2003) Acclimation capacity underlies susceptibility to climate change. Science 301:65

    Article  CAS  Google Scholar 

  • Storm L, Pedersen SA (2003) Development and drift of northern shrimp larvae (Pandalus borealis) at West Greenland. Mar Biol 143:1083–1093

    Article  Google Scholar 

  • Sunday JM, Crim RN, Harley CDG, Hart MW (2011) Quantifying rates of evolutionary adaptation in response to ocean acidification. PLoS ONE 6:e22881

    Article  CAS  Google Scholar 

  • Taylor AC, Spicer JI (1989) Interspecific comparison of the respiratory response to declining oxygen tension and the oxygen transporting properties of the blood of some palaemonid prawns (Crustacea: Palaemonidae). Mar Behav Physiol 14:81–91

    Article  Google Scholar 

  • Thorson G (1950) Reproductive and larval ecology of marine bottom invertebrates. Biol Rev 25:1–45

    Article  Google Scholar 

  • Walther K, Anger K, Pörtner HO (2010) Effects of ocean acidification and warming on the larval development of the spider crab Hyas araneus from different latitudes (54 vs. 79°N). Mar Ecol Prog Ser 417:159–170

    Article  Google Scholar 

  • Weinberg R (1982) Studies on the influence of temperature, salinity, light and feeding rate on laboratory reared larvae of deep sea shrimp, Pandalus borealis Krøyer 1838. Meeresforsch Rep Mar Res 29:136–153

    Google Scholar 

  • Whiteley NM (2011) Physiological and ecological responses of crustaceans to ocean acidification. Mar Ecol Prog Ser 430:257–271

    Article  CAS  Google Scholar 

  • Widdicombe S, Needham HR (2007) Impact of CO2-induced seawater acidification on the burrowing activity of Nereis virens and sediment nutrient flux. Mar Ecol Prog Ser 341:111–122

    Article  Google Scholar 

  • Widdows J (1991) Physiological ecology of mussel larvae. Aquaculture 94:147–163

    Article  Google Scholar 

  • Wood HL, Spicer JI, Kendall MA, Lowe DM, Widdicombe S (2011) Ocean warming and acidification; implications for the Arctic brittlestar Ophiocten sericeum. Polar Biol 34:1033–1044

    Article  Google Scholar 

Download references

Acknowledgments

We thank Anna Ingvarsdottir and Ingrid.C.Taban at IRIS (International Research Institute of Stavanger) for help and technical support. This study was funded by The Research Council of Norway (RCN) through two projects: ‘Combined effects of ocean acidification, climate change and oil related discharges’ (200800/S40) and IRIS-anchored strategic project ‘Effects of ocean acidification on invertebrate calcifying larvae’. The experiments were performed at Akvamiljo, the marine research facility of IRIS. This work was undertaken whilst MA was undertaking her doctorate study at IRIS/Plymouth University, and PC was in receipt of a Research Council UK Research Fellowship to investigate ocean acidification at the Plymouth University.

Author information

Authors and Affiliations

  1. Marine Biology and Ecology Research Centre, School of Marine Science and Engineering, Plymouth University, Drake Circus, Plymouth, Devon, PL4 8AA, UK

    Maj Arnberg, Piero Calosi & John I. Spicer

  2. IRIS-International Research Institute of Stavanger, Mekjarvik 12, 4070, Randaberg, Norway

    Maj Arnberg, Anne Helene S. Tandberg, Marianne Nilsen, Stig Westerlund & Renée K. Bechmann

Authors
  1. Maj Arnberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Piero Calosi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. John I. Spicer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Anne Helene S. Tandberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Marianne Nilsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Stig Westerlund
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Renée K. Bechmann
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maj Arnberg.

Additional information

Communicated by S. Dupont.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Arnberg, M., Calosi, P., Spicer, J.I. et al. Elevated temperature elicits greater effects than decreased pH on the development, feeding and metabolism of northern shrimp (Pandalus borealis) larvae. Mar Biol 160, 2037–2048 (2013). https://doi.org/10.1007/s00227-012-2072-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-012-2072-9

Keywords

Search

Navigation