, Volume 159, Issue 2, pp 257–269 | Cite as

Variation in immune defence among populations of Gammarus pulex (Crustacea: Amphipoda)

Population Ecology - Original Paper


Despite intensive studies in ecological immunology, few have investigated variation in immune defence among natural populations; in particular, there is a lack of knowledge of the sources of spatial variability in immune defence in the wild. Here we documented variation among twelve populations of the freshwater crustacean Gammarus pulex in the activity of the prophenoloxidase (ProPO) system, which is an important component of invertebrate immunity. We then tested for trade-offs between investment in immune defence and fitness-related traits such as survival and fecundity, as well as for environmental causes of variability (water temperature and conductivity, parasite prevalence). Levels of immune defence differed among populations, with environment partly explaining this population effect, as immune activities were negatively related to water conductivity and acanthocephalan parasite prevalence. There was a strong variation among populations for the maintenance of the ProPO system, while variation in its use was relatively weak. Such a pattern could be partly explained by the relative costs associated with the maintenance and/or the use of the ProPO system. Investment in the ProPO system was negatively correlated to survival, whereas it was positively related to female fecundity and resource storage. However, variation in immunity did not predict resistance to bacterial infection among populations, suggesting that measuring the activity of the ProPO system might not be sufficient to estimate immunocompetence at the population level. These results suggest that investment in immune function is a variable trait, which might be locally optimized as a result of both life history trade-offs and environmental conditions, highlighting the need to combine them in a common framework.


Acanthocephalans Ecological immunology Immunocompetence Life history traits Phenoloxidase 



We thank G. Sorci, S. Morand, T. Rigaud and M. J. F. Brown for critical reading and comments on previous drafts of the manuscript. This study was supported by a grant from the Conseil Régional de Bourgogne within the programme FABER (Favoriser l’Accueil en Bourgogne d’Equipes de Recherches) and the CNRS (Centre National de la Recherche Scientifique). This experiment complies with the current laws of France.


  1. Adamo SA (2004a) Estimating disease resistance in insects: phenoloxidase and lysozyme-like activity and disease resistance in the cricket Gryllus texensis. J Insect Physiol 50:209–216PubMedCrossRefGoogle Scholar
  2. Adamo SA (2004b) How should behavioural ecologists interpret measurements of immunity? Anim Behav 68:1443–1449CrossRefGoogle Scholar
  3. Agnew PC, Koella J, Michalakis Y (2000) Host life history responses to parasitism. Microbes Infect 2:891–896PubMedCrossRefGoogle Scholar
  4. Ahmed AM, Baggot SL, Maingon R, Hurd H (2002) The cost of mounting an immune response are reflected in the reproductive fitness of the mosquito Anopheles gambiae. Oikos 97:371–377CrossRefGoogle Scholar
  5. Armitage SAO, Thompson JJW, Rolff J, Siva-Jothy MT (2003) Examining costs of induced and constitutive immune investment in Tenebrio molitor. J Evol Biol 16:1038–1044PubMedCrossRefGoogle Scholar
  6. Bachère E (2000) Shrimp immunity and disease control. Aquaculture 191:3–11CrossRefGoogle Scholar
  7. Bai GX, Johnston LA, Watson CO, Yoshino TP (1997) Phenoloxidase activity in the reproductive system of Biomphalaria glabrata: role in egg production and effect of schistosome infection. J Parasitol 83:852–858PubMedCrossRefGoogle Scholar
  8. Barnes AI, Siva-Jothy MT (2000) Density-dependent prophylaxis in the mealworm beetle Tenebrio molitor L. (Coleoptera: Tenebrionidae): cuticular melanization is an indicator of investment in immunity. Proc R Soc Lond B 267:177–182CrossRefGoogle Scholar
  9. Blount JD, Houston DC, Møller AP, Wright J (2003) Do individual branches of immune defence correlate? A comparative case study of scavenging and non-scavenging birds. Oikos 102:340–350CrossRefGoogle Scholar
  10. Bollache L, Rigaud T, Cézilly F (2002) Effects of two acanthocephalan parasites on the fecundity and pairing status of female Gammarus pulex (Crustacea: Amphipoda). J Invertebr Pathol 79:102–110PubMedCrossRefGoogle Scholar
  11. Bonneaud C et al. (2003) Assessing the cost of mounting an immune response. Am Nat 161:367–379Google Scholar
  12. Bryan-Walker K, Leung TLF, Poulin R (2007) Local adaptation of immunity against a trematode parasite in marine amphipod populations. Marine Biol 152:687–695CrossRefGoogle Scholar
  13. Butt D, Aladaileh S, O’Connor WA, Raftos DA (2007) Effect of starvation on biological factors related to immunological defence in the Sydney rock oyster (Saccostrea glomerata). Aquaculture 264:82–91CrossRefGoogle Scholar
  14. Cerenius L, Söderhäll K (2004) The prophenoloxidase-activating system in invertebrates. Immunol Rev 198:116–126PubMedCrossRefGoogle Scholar
  15. Cézilly F, Grégoire A, Bertin A (2000) Conflict between co-occuring manipulative parasites? An experimental study of the joint influence of two acanthocephalan parasites on the behaviour of Gammarus pulex. Parasitology 120:625–630PubMedCrossRefGoogle Scholar
  16. Cornet S, Biard C, Moret Y (2007) Is there a role for antioxidant carotenoids in limiting self-harming immune response in invertebrates? Biol Lett 3:284–288PubMedCrossRefGoogle Scholar
  17. Cornet S, Franceschi N, Bauer A, Rigaud T, Moret Y (2008) Immune depression induced by acanthocephalan parasites in their intermediate crustacean host: consequences for the risk of super-infection and links with host behavioural manipulation. Int J Parasitol (in press)Google Scholar
  18. Cotter SC, Kruuk LEB, Wilson K (2004) Costs of resistance: genetic correlations and potential trade-offs in an insect immune system. J Evol Biol 17:421–429PubMedCrossRefGoogle Scholar
  19. Da Silva CCA (2002) Activation of the prophenoloxidase and removal of Bacillus subtilis from the hemolymph of Acheta domesticus (L.) (Orthoptera: Gryllidae). Neotrop Entomol 31:487–491Google Scholar
  20. Demas GE, Chefer V, Talan MI, Nelson RJ (1997) Metabolic costs of mounting an antigen-stimulated immune response in adult and aged C57BL/6 J mice. Am J Physiol 273:R1631–R1637PubMedGoogle Scholar
  21. Gillespie JP, Kanost MR, Trenczek T (1997) Biological mediators of insect immunity. Annu Rev Entomol 42:611–643PubMedCrossRefGoogle Scholar
  22. Glazier DS, Sparks BL (1997) Energetics of amphipods in ion-poor waters: stress resistance is not invariably linked to low metabolic rates. Funct Ecol 11:126–128CrossRefGoogle Scholar
  23. Gonzalez G, Sorci G, Møller AP, Ninni P, Haussy C, De Lope F (1999) Immunocompetence and condition-dependent sexual advertisement in male house sparrows (Passer domesticus). J Anim Ecol 68:1225–1234CrossRefGoogle Scholar
  24. Goüy De Bellocq J, Porcherie A, Moulia C, Morand S (2007) Immunocompetence does not correlate with resistance to helminth parasites in house mouse subspecies and their hybrids. Parasitol Res 100:321–328PubMedCrossRefGoogle Scholar
  25. Hanssen SA, Hasselquist D, Folstad I, Erikstad KE (2004) Cost of immunity: immune responsiveness reduces survival in a vertebrate. Proc R Soc Lond B 271:925–930CrossRefGoogle Scholar
  26. Harris RR, Aladin NV (1997) The ecophysiology of osmoregulation in Crustacea. In: Hazon N, Eddy FB, Flik G (eds) Ionic regulation in animals. Springer, Berlin, pp 1–25Google Scholar
  27. Hillyer JF, Christensen BM (2005) Mosquito phenoloxidase and defensin colocalize in melanization innate immune responses. J Histochem Cytochem 53:689–698PubMedCrossRefGoogle Scholar
  28. Ilmonen P, Taarna T, Hasselquist D (2000) Experimentally activated immune defence in female pied flycatchers results in reduced breeding success. Proc R Soc Lond B 267:663–670CrossRefGoogle Scholar
  29. Jacot A, Scheuber H, Brinkhof MWG (2004) Costs of an induced immune response on sexual display and longevity in field crickets. Evolution 58:2280–2286PubMedGoogle Scholar
  30. Jokela J, Schmid-Hempel P, Rigby MC (2000) Dr. Pangloss restrained by the red queen––steps towards a unified defence theory. Oikos 89:267–274CrossRefGoogle Scholar
  31. Kalbe M, Kurtz J (2006) Local differences in immunocompetence reflect resistance of sticklebacks against the eye fluke Diplostomum pseudospathaceum. Parasitology 132:105–116PubMedCrossRefGoogle Scholar
  32. Kefford BJ, Papas PJ, Nugegoda D (2003) Relative salinity tolerance of macroinvertebrates from the Barwon River, Victoria. Mar Freshwater Res 54:755–765Google Scholar
  33. Kraaijeveld AR, Van Alphen JJM (1995) Geographic variation in encapsulation ability of Drosophila melanogaster larvae and evidence for parasitoid-specific components. Evol Ecol 9:10–17CrossRefGoogle Scholar
  34. Lagrue C, Kaldonski N, Perrot-Minnot MJ, Motreuil S, Bollache L (2007) Modification of host’s behavior by a parasite: field evidence for adaptive manipulation. Ecology 88:2839–2847PubMedCrossRefGoogle Scholar
  35. Lambrechts L, Vulule J, Koella JC (2004) Genetic correlation between melanization and antibacterial immune responses in a natural population of the malaria vector Anopheles gambia. Evolution 58:2377–2381PubMedGoogle Scholar
  36. Le Moullac G, Haffner P (2000) Environmental factors affecting immune responses in Crustacea. Aquaculture 191:121–131CrossRefGoogle Scholar
  37. Lee KP, Cory JS, Wilson K, Raubenheimer D, Simpson SJ (2005) Flexible diet choice protein costs of pathogen resistance in a caterpillar. Proc Roy Soc B 273:823–829CrossRefGoogle Scholar
  38. Li J, Christensen BM (1993) Involvement of L-tyrosine and phenoloxidase in the tanning of Aedes aegypti eggs. Insec Biochem Mol Biol 23:739–748Google Scholar
  39. Lindström KM, Foufopoulos J, Pärn H, Wikelski M (2004) Immunological investments reflect parasite abundance in island populations of Darwin’s finches. Proc R Soc Lond B 271:1513–1519CrossRefGoogle Scholar
  40. Little TJ, Killick SC (2007) Evidence for a cost of immunity when the crustacean Daphnia magna is exposed to the bacterial pathogen Pasteuria ramosa. J Anim Ecol 76:1202–1207PubMedCrossRefGoogle Scholar
  41. Little TJ, Hultmark D, Read AF (2005) Invertebrate immunity and the limits of mechanistic immunology. Nature Immunol 6:651–654CrossRefGoogle Scholar
  42. Lochmiller RL, Vestey MR, Boren JC (1993) Relationship between protein nutritional status and immunocompetence in northern bobwhite chicks. The Auk 110:503–510Google Scholar
  43. Martin LB, Scheuerlein A, Wikelski M (2003) Immune activity elevates energy expenditure of house sparrows: a link between direct and indirect costs? Proc R Soc Lond B 270:153–158CrossRefGoogle Scholar
  44. Mayrand E, St-Jean SD, Courtenay SC (2005) Haemocyte responses of blue mussels (Mytilus edulis L.) transferred from a contaminated site to a reference site: can the immune system recuperate? Aquaculture Res 36:962–971CrossRefGoogle Scholar
  45. Meyran JC, Gielly L, Taberlet P (1998) Environmental calcium and mitochondrial DNA polymorphism among local populations of Gammarus fossarum (Crustacea, Amphipoda). Mol Ecol 7:1391–1400CrossRefGoogle Scholar
  46. Moret Y, Schmid-Hempel P (2000) Survival for immunity: the price of immune system activation for bumblebee workers. Science 290:1166–1168PubMedCrossRefGoogle Scholar
  47. Mucklow PT, Vizoso DB, Jensen KH, Refardt D, Ebert D (2004) Variation in phenoloxidase activity and its relation to parasite resistance wihin and between populations of Daphnia magna. Proc R Soc Lond B 271:1175–1183CrossRefGoogle Scholar
  48. Müller J, Partsch E, Link A (2000) Differentiation in morphology and habitat partitioning of genetically characterized Gammarus fossarum forms (Amphipoda) across a contact zone. Biol J Lin Soc 69:41–53CrossRefGoogle Scholar
  49. Mydlarz LD, Jones LE, Harvell CD (2006) Innate immunity, environmental drivers and disease ecology of marine and freshwater invertebrates. Annu Rev Ecol Evol Syst 37:251–288CrossRefGoogle Scholar
  50. Nigam Y, Maudlin I, Welburn S, Ratcliffe NA (1997) Detection of phenoloxidase activity in the hemolymph of tsetse flies, rafractory and succeptible to infection with Trypanosoma brucei rhodesiense. J Invertebr Pathol 69:279–281PubMedCrossRefGoogle Scholar
  51. Ots I, Kerimov AB, Ivankina E, Ilyina TA, Hõrak P (2001) Immune challenge affects basal metabolic activity in wintering great tits. Proc R Soc Lond B 268:1175–1181CrossRefGoogle Scholar
  52. Owen IPF, Wilson K (1999) Immunocompetence: a neglected life history trait or conspicuous red herring? Trends Ecol Evol 14:170–172CrossRefGoogle Scholar
  53. Perrot-Minnot M-J (2004) Larval morphology, genetic divergence, and contrasting levels of host manipulation between forms of Pomphorhynchus laevis (Acanthocephala). Int J Parasitol 34:45–54PubMedCrossRefGoogle Scholar
  54. Plaistow SJ, Troussard J-P, Cézilly F (2001) The effect of the acanthocephalan parasite Pomphorhynchus laevis on the lipid and glycogen content of its intermediate host Gammarus pulex. Int J Parasitol 31:346–351PubMedCrossRefGoogle Scholar
  55. Reznick D, Nunney L, Tessier A (2000) Big houses, big cars, superfleas and the cost of reproduction. Trends Ecol Evol 15:421–425PubMedCrossRefGoogle Scholar
  56. Rigaud T, Moret Y (2003) Differential phenoloxidase activity between native and invasive gammarids infected by local acanthocephalans: differential immunosuppression? Parasitology 127:571–577PubMedCrossRefGoogle Scholar
  57. Rolff J, Siva-Jothy MT (2004) Selection on insect immunity in the wild. Proc R Soc Lond B 271:2157–2160CrossRefGoogle Scholar
  58. Sandland G, Minchella DJ (2003) Costs of immune defence: an enigma wrapped in an environmental cloak? Trends Parasitol 19:571–574PubMedCrossRefGoogle Scholar
  59. Schmid-Hempel P (2003) Variation in immune defence as a question of evolutionary ecology. Proc R Soc Lond B 270:357–366CrossRefGoogle Scholar
  60. Schwartz A, Koella JC (2004) The cost of immunity in the yellow fever mosquito, Aedes aegypti depends on immune activation. J Evol Biol 17:834–840PubMedCrossRefGoogle Scholar
  61. Schwarzenbach GA, Ward PI (2007) Phenoloxidase activity and pathogen resistance in yellow dung flies Scathophaga stercoraria. J Evol Biol 20:2192–2199PubMedCrossRefGoogle Scholar
  62. Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321CrossRefGoogle Scholar
  63. Siva-Jothy MT (2000) A mechanistic link between parasite resistance and expression of a sexually selected trait in a damselfly. Proc R Soc Lond B 267:2523–2527CrossRefGoogle Scholar
  64. Siva-Jothy MT, Thompson JJW (2002) Short-term nutrient deprivation affects immune function. Physiol Entomol 27:206–212CrossRefGoogle Scholar
  65. Siva-Jothy MT, Moret Y, Rolff J (2005) Insect immunity: an evolutionary ecology perspective. Adv Insect Physiol 32:1–48CrossRefGoogle Scholar
  66. Sugumaran M, Nellaiappan K, Valivittan K (2000) A new mechanism for the control of phenoloxidase activity: inhibition and complex formation with quinone isomerase. Arch Biochem Biophys 379:252–260PubMedCrossRefGoogle Scholar
  67. Sung HH, Huang Y-T, Hsiao L-T (2004) Phenoloxidase activity of Macrobrachium rosenbergii after challenge with two kinds of pathogens: Lactococcus garvieae and Aeromonas veronii. Fish Pathol 39:1–8Google Scholar
  68. Sutcliffe DW (1993) Reproduction in Gammarus (Crustacea Amphipoda): female strategies. Freshwater Forum 3:26–65Google Scholar
  69. Svensson E, Råberg L, Koch C, Hasselquist D (1998) Energetic stress, immunosuppression and the costs of an antibody response. Funct Ecol 12:912–919CrossRefGoogle Scholar
  70. Tinsley MC, Blanford S, Jiggins FM (2006) Geographic variation in Drosophila melanogaster pathogen susceptibility. Parasitology 132:767–773PubMedCrossRefGoogle Scholar
  71. Tschirren B, Richner H (2006) Parasites shape the optimal investment in immunity. Proc Roy Soc B 273:1773–1777CrossRefGoogle Scholar
  72. Wakelin D (1996) Immunity to parasites: how parasitic infections are controlled, 2nd edn. Cambridge University Press, CambridgeGoogle Scholar
  73. Zuk M, Stoehr AM (2002) Immune defense and host life history. Am Nat 160:S9–S22PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Stéphane Cornet
    • 1
  • Clotilde Biard
    • 1
    • 2
  • Yannick Moret
    • 1
  1. 1.UMR CNRS 5561 Biogéosciences, Équipe Écologie ÉvolutiveUniversité de BourgogneDijonFrance
  2. 2.Konrad Lorenz Institute for EthologyAustrian Academy of SciencesViennaAustria

Personalised recommendations