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A summer heat wave decreases the immunocompetence of the mesograzer, Idotea baltica

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Abstract

Extreme events associated with global change will impose increasing stress on coastal organisms. How strong biological interactions such as the host–parasite arms-race are modulated by environmental change is largely unknown. The immune system of invertebrates, in particular phagocytosis and phenoloxidase activity response are key defence mechanisms against parasites, yet they may be sensitive to environmental perturbations. We here simulated an extreme event that mimicked the European heat wave in 2003 to investigate the effect of environmental change on the immunocompetence of the mesograzer Idotea baltica. Unlike earlier studies, our experiment aimed at simulation of the natural situation as closely as possible by using long acclimation, a slow increase in temperature and a natural community setting including the animals’ providence with natural food sources (Zostera marina and Fucus vesiculosus). Our results demonstrate that a simulated heat wave results in decreased immunocompetence of the mesograzer Idotea baltica, in particular a drop of phagocytosis by 50%. This suggests that global change has the potential to significantly affect host–parasite interactions.

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References

  • Altizer S, Harvell D, Friedle E (2003) Rapid evolutionary dynamics and disease threats to biodiversity. Trends Ecol Evol 18:589–596

    Article  Google Scholar 

  • Asshoff R, Hättenschwiler S (2005) Growth and reproduction of the alpine grasshoper Miramella alpina feeding on CO2 enriched dwarf shrubs at treeline. Oecologia 142:191–201

    Article  Google Scholar 

  • Bachere E, Miahle E, Rodriguez J (1995) Identification of defence effectors in the haemolymph of crustaceans with particular reference to the shrimp Penaeus japonicus (Bate): prospects and application. Fish Shellfish Immun 5:137–143

    Article  Google Scholar 

  • Bateman AJ (1948) Intra-sexual selection in Drosophila. Heredity 2:349–368

    Article  CAS  Google Scholar 

  • Belkin IM (2009) Rapid warming of large marine ecosystems. Prog Oceanogr 81:207–213

    Article  Google Scholar 

  • Blanford S, Thomas MT, Pugh C, Pell JK (2003) Temperature checks the Red Queen? Resistance and virulence in a fluctuating environment. Ecol Lett 6:2–5

    Article  Google Scholar 

  • Boots M, Bowers RG (2004) The evolution of resistance through costly acquired immunity. Proc R Soc Lond Ser B 271:715–723

    Article  Google Scholar 

  • Chen JC, Lin MN, Ting YY, Lin JN (1995) Survival, haemolymph osmolarity and tissue water of Penaeus chinensis juveniles acclimated to different salinities and temperature levels. Comp Biochem Physiol 110:253–258

    Article  Google Scholar 

  • Cheng W, Chen S-M, Want F-I, Hsu P-I, Liu C-H, Chen J-C (2003) Effects of temperature, pH, salinity and ammonia on the phagocytic activity and clearance efficiency of giant freshwater prawn Macrobrachium rosenbergii to Lactococcus garvieae. Aquaculture 219:111–121

    Article  Google Scholar 

  • Clutton-Brock TH (1988) Reproductive success. University of Chicago Press, Chicago

  • Dove ADM, Allam B, Powers JJ, Sokolowski MS (2005) A prolonged thermal stress experiment on the American lobster, Homarus americanus. J Shellfish Res 24:761–765

    Google Scholar 

  • Franke H-D, Janke M (1998) Mechanisms and consequences of intra- and interspecific interference competition in Idotea baltica (Pallas) and Idotea emarginata (Fabricius) (Crustacea: Isopoda): a laboratory study of possible proximate causes of habitat segregation. J Exp Mar Biol Ecol 227:1–21

    Article  Google Scholar 

  • Franke H-D, Gutow L, Janke M (1999) The recent arrival of the oceanic isopod Idotea metalica Box off Helgoland (German Bight, North Sea): an indication of a warming trend in the North Sea? Helgolander Meeresun 52:347–357

    Google Scholar 

  • Franke H-D, Gutow L, Janke M (2007) Flexible habitat selection and interactive habitat segregation in the marine congeners Idotea baltica and Idotea emarginata (Crustacea, Isopoda). Mar Biol 150:929–939

    Article  Google Scholar 

  • Frich P, Alexander LV, Della-Marta P, Gleason B, Haylock M, Tank A, Peterson T (2002) Observed coherent changes in climatic extremes during the second half of the twentieth century. Climate Res 19:193–212

    Article  Google Scholar 

  • Gomulkiewicz R, Thompson JN, Holt RD, Nuismer SL, Hochberg ME (2000) Hot spots, cold spots, and the geographic mosaic theory of coevolution. Am Nat 156:156–174

    Article  Google Scholar 

  • Gutow L, Strahl J, Wiencke C, Franke H-D, Saborowski R (2006) Behavioural and metabolic adaptations of marine isopods to the rafting life style. Mar Biol 149:821–828

    Article  Google Scholar 

  • Gutow L, Leidenberger S, Boos K, Franke H-D (2007) Differential life history response of two Idotea species (Crustacea: Isopoda) to food limitation. Mar Ecol Prog Ser 344:159–172

    Article  Google Scholar 

  • Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, Samuel MD (2002) Climate warming and disease risks for terrestrial and marine biota. Science 296:2158–2162

    Article  CAS  Google Scholar 

  • Hemmi A, Jormalainen V (2002) Nutrient enhancement increases performance of a marine herbivore via quality of its food algae. Ecology 83:1052–1064

    Article  Google Scholar 

  • Hoch G, Popp M, Körner C (2002) Altitudinal increase of mobile carbon pools in Pinus cembra suggests sink limitation of growth at the Swiss treeline. Oikos 98:361–374

    Article  CAS  Google Scholar 

  • Hoffmann JA (2003) The immune response of Drosophila. Nature 426:33–38

    Article  CAS  Google Scholar 

  • IPCC (2007) Climate change 2007: synthesis report: summary for policymakers

  • Irmak P, Kurtz J, Zimmer M (2005) Immune response in Porcellio scaber (Isopoda: Oniscidea) copper revisited. Eur J Soil Biol 41:77–83

    Article  CAS  Google Scholar 

  • Jaenicke E, Fraune S, May S, Irmak P, Augustin R, Meesters C, Decker H, Zimmer M (2009) Is activated hemocyanin instead of phenoloxidase involved in immune response in woodlice? Dev Comp Immunol 33:1055–1063

    Article  CAS  Google Scholar 

  • Janeway CA, Medzhitov R (2002) Innate immune recognition. Ann Rev Immunol 20:197–216

    Article  CAS  Google Scholar 

  • Jaschinski S, Sommer U (2008) Functional diversity of mesograzers in an eelgrass-epiphyte system. Mar Biol 154:475–482

    Article  Google Scholar 

  • Jutras I, Desjardins M (2005) Phagocytosis: at the crossroads of innate and adaptive immunity. Annu Rev Cell Dev Biol 21:511–527

    Article  CAS  Google Scholar 

  • Karowe DN (2007) Are legume-feeding herbivores buffered against direct effects of elevated carbon dioxide on host plants? A test with the sulfur butterfly, Colias philodice. Glob Change Biol 13:2045–2051

    Article  Google Scholar 

  • Kaspar CW, Tampling ML (1993) Effects of temperature and salinity on the survival of Vibrio vunificus in seawater and shellfish. Appl Environ Microbiol 59:2425–2429

    CAS  Google Scholar 

  • Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241

    Article  Google Scholar 

  • Kurtz J (2002) Phagocytosis by invertebrate hemocytes: causes of individual variation in Panorpa vulgaris scorpionflies. Microsc Res Tech 57:465–468

    Article  Google Scholar 

  • Kurtz J, Franz K (2003) Evidence for memory in invertebrate immunity. Nature 425:37–38

    Article  CAS  Google Scholar 

  • Kurtz J, Sauer K (1999) The immunocompetence handicap hypothesis: testing the genetic predictions. Proc R Soc Lond Ser B 266:2515–2522

    Article  Google Scholar 

  • Kurtz J, Wiesner A, Gotz P, Sauer KP (2000) Gender differences and individual variation in the immune system of the scorpionfly Panorpa vulgaris (Insecta : Mecoptera). Dev Comp Immunol 24:1–12

    Article  CAS  Google Scholar 

  • Moullac G, Haffner P (2000) Environmental factors affecting immune responses in Crustacea. Aquaculture 191:121–131

    Article  Google Scholar 

  • Mydlarz LD, Jones LE, Havell CD (2006) Innate immunity, environmental drivers and disease ecology of marine and freshwater invertebrates. Annu Rev Ecol Evol Syst 37:251–288

    Article  Google Scholar 

  • Reusch TBH, Eherls A, Hammerli A, Worm B (2005) Ecosystem recovery after climatic extremes enhanced by genotypic diversity. Proc Natl Acad Sci USA 102:2826–2831

    Article  CAS  Google Scholar 

  • Robohm RA, Draxler AFJ, Wieczorek D, Kapareiko D, Pitchford S (2005) Effects of environmental stressors on disease susceptibility in American lobsters: a controlled laboratory study. J Shellfish Res 24:773–779

    Google Scholar 

  • Rolff J (2002) Bateman′s principle and immunity. Proc R Soc Lond Ser B 269:867–872

    Article  Google Scholar 

  • Rosenberg E, Ben-Haim Y (2002) Microbial diseases of corals and global warming. Environ Microbiol 4:318–326

    Article  Google Scholar 

  • Roth O, Kurtz J (2009) Phagocytosis mediates specificity in the immune defence of an invertebrate, the woodlouse Porcellio scaber (Crustacea: Isopoda). Dev Comp Immunol 33:11151–11155

    Article  Google Scholar 

  • Roth O, Sadd BM, Schmid-Hempel P, Kurtz J (2009) Strain-specific priming of resistance in the red flour beetle, Tribolium castaneum. Proc R Soc Lond Ser B 276:145–151

    Article  Google Scholar 

  • Ryder J, Siva-Jothy MT (2000) Male calling song provides a reliable signal of immune function in a cricket. Proc R Soc Lond Ser B 263:1171–1175

    Article  Google Scholar 

  • Sadd BM, Schmid-Hempel P (2006) Insect immunity shows specificity in protection upon secondary pathogen exposure. Curr Biol 16:1206–1210

    Article  CAS  Google Scholar 

  • Schar C, Jendritzky G (2004) Climate change: hot news from summer 2004. Nature 432:559–560

    Article  Google Scholar 

  • Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321

    Article  CAS  Google Scholar 

  • Skarstein F, Folstad I (1996) Sexual dichromatism and the immunocompetence handicap: an observational approach using Arctic charr. Oikos 76:359–367

    Article  Google Scholar 

  • Staples DJ, Heales DS (1991) Temperature and salinity optima for growth and survival of juvenile banana prawns Penaeus merguiensis. Aquaculture 14:23–30

    Google Scholar 

  • Steenbergen JF, Steenbergen SM, Schapiro HC (1978) Effects of temperature on phagocytosis in Homarus americanus. Aquaculture 14:23–30

    Article  Google Scholar 

  • Thomas MB, Blanford S (2003) Thermal bioloy in insect-parasite interactions. Trends Ecol Evol 18:344–350

    Article  Google Scholar 

  • Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008) Global change and species interactions in terrestrial ecosystems. Ecol Lett 11:1351–1363

    Article  Google Scholar 

  • Verhulst S, Dieleman S, Parmentier H (1999) A tradeoff between immunocompetence and sexual ornamentation in domestic fowl. Proc Natl Acad Sci USA 96:4478–4481

    Article  CAS  Google Scholar 

  • Veteli TO, Kuokkanen K, Julkunen-Tiitto R, Roininen H, Tahvanainen J (2002) Effects of elevated CO2 and temperature on plant growth and herbivore defensive chemistry. Glob Change Biol 8:1240–1252

    Article  Google Scholar 

  • Williams SL, Ruckelhaus MH (1993) Effects of nitrogen availability and herbivory on eelgrass (Zostera marina) and epiphytes. Ecology 74:904–918

    Article  Google Scholar 

Download references

Acknowledgments

We want to thank Günter Hoch from the University of Basel for analysing leaf content. Without the “Aquatron-team” that provided the facility and the technical support this experiment would have not been accomplished, many thanks to Peter Nelle, Birgit Fricke, Nina Bergmann and Gidon Winters. We are grateful for the help of Roman Asshoff during the experiment. We thank Gisep Rauch for comments on an earlier version of this manuscript. This study was supported by a grant from the Swiss National Science Foundation (3100A0-112992 to J.K.). O.R. was supported by the Volkswagen Stiftung.

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Authors and Affiliations

  1. Institute for Evolution and Biodiversity, Westfälische Wilhelms-Universität Münster, Hüfferstrasse 1, 48149, Münster, Germany

    Olivia Roth, Joachim Kurtz & Thorsten B. H. Reusch

  2. Institute for Integrative Biology, Experimental Ecology, Universitätsstrasse 16, ETH-Zentrum, 8092, Zürich, Switzerland

    Olivia Roth

  3. Leibniz Institute for Marine Sciences, IFM-Geomar, Evolutionary Ecology of Marine Fishes, Düsternbrooker Weg 20, 24105, Kiel, Germany

    Olivia Roth & Thorsten B. H. Reusch

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  1. Olivia Roth
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  2. Joachim Kurtz
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Correspondence to Olivia Roth.

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Communicated by H. O. Pörtner.

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Roth, O., Kurtz, J. & Reusch, T.B.H. A summer heat wave decreases the immunocompetence of the mesograzer, Idotea baltica . Mar Biol 157, 1605–1611 (2010). https://doi.org/10.1007/s00227-010-1433-5

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  • DOI: https://doi.org/10.1007/s00227-010-1433-5

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