Parasitology Research

, Volume 109, Issue 3, pp 759–767 | Cite as

Variation of parasite load and immune parameters in two species of New Zealand shore crabs

  • Jessica DittmerEmail author
  • Anson V. Koehler
  • Freddie-Jeanne Richard
  • Robert Poulin
  • Mathieu Sicard
Original Paper


While parasites are likely to encounter several potential intermediate hosts in natural communities, a parasite’s actual range of compatible hosts is limited by numerous biological factors ranging from behaviour to immunology. In crustaceans, two major components of immunity are haemocytes and the prophenoloxidase system involved in the melanisation of foreign particles. Here, we analysed metazoan parasite prevalence and loads in the two sympatric crab species Hemigrapsus crenulatus and Macrophthalmus hirtipes at two sites. In parallel, we analysed the variation in haemocyte concentration and amount of circulating phenoloxidase (PO) in the haemolymph of the same individuals in an attempt to (a) explain differences in parasite prevalence and loads in the two species at two sites and (b) assess the impact of parasites on these immune parameters. M. hirtipes harboured more parasites but also exhibited higher haemocyte concentrations than H. crenulatus independent of the study site. Thus, higher investment in haemocyte production for M. hirtipes does not seem to result in higher resistance to parasites. Analyses of variation in immune parameters for the two crab species between the two sites that differed in parasite prevalence showed common trends. (a) In general, haemocyte concentrations were higher at the site experiencing higher parasitic pressure while circulating PO activity was lower and (b) haemocyte concentrations were influenced by microphallid trematode metacercariae in individuals from the site with higher parasitic pressure. We suggest that the higher haemocyte concentrations observed in both crab species exposed to higher parasitic pressure may represent an adaptive response to the impact of parasites on this immune parameter.


Parasite Prevalence Sodium Cacodylate Buffer Carapace Width Immune Parameter Crab Species 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



The authors would like to thank the entire parasitology research group at the University of Otago; Karen Judge for providing equipment; Charlotte Seifert for assistance during field work and Jean-Baptiste Ferdy as well as Ning Liu for help with the programming in R. This project was funded by the Erasmus Mundus Program “European Master in Applied Ecology” (EMAE).


  1. Adamson ML, Caira JN (1994) Evolutionary factors influencing the nature of parasite specificity. Parasitology 109:S85–S95PubMedCrossRefGoogle Scholar
  2. Brockerhoff AM, Smales LR (2002) Profilicolllis novaezelandensis n. sp. (Polymorphidae) and two other acanthocephalan parasites from shore birds (Haematopodidae and Scolopacidae) in New Zealand, with records of two species in intertidal crabs (Decapoda: Grapsidae and Ocypodidae). Syst Parasitol 52:55–65PubMedCrossRefGoogle Scholar
  3. Bryan-Walker K, Leung TLF, Poulin R (2007) Local adaptation of immunity against a trematode parasite in marine amphipod populations. Mar Biol 152:687–695CrossRefGoogle Scholar
  4. Cerenius L, Söderhäll K (2004) The prophenoloxidase-activating system in invertebrates. Immunol Rev 198:116–126PubMedCrossRefGoogle Scholar
  5. Cerenius L, Lee BL, Söderhäll K (2008) The proPO-System: pros and cons for its role in invertebrate immunity. Trends Immunol 29:263–271PubMedCrossRefGoogle Scholar
  6. Cerenius L, Babu R, Söderhäll K, Jiravanichpaisal P (2010) In vitro effects on bacterial growth of phenoloxidase reaction products. J Invertebr Pathol 103:21–23PubMedCrossRefGoogle Scholar
  7. Chisholm JRS, Smith VJ (1992) Antibacterial activity in the haemocytes of the shore crab, Carcinus maenas. J Mar Biol Assoc UK 72:529–542CrossRefGoogle Scholar
  8. Combes C (2001) Parasitism. The ecology and evolution of intimate interactions. University of Chicago Press, ChicagoGoogle Scholar
  9. Cornet S, Biard C, Moret Y (2009) Variation in immune defence among populations of Gammarus pulex (Crustacea: Amphipoda). Oecologia 159:257–269PubMedCrossRefGoogle Scholar
  10. Damian RT (1997) Parasite immune evasion and exploitiation: reflections and projections. Parasitology 115:S169–S175PubMedCrossRefGoogle Scholar
  11. Destoumieux D, Bulet P, Loew D, Van Dorsselaer A, Rodriguez G, Bachère E (1997) Penaeidins, a new family of antimicrobial peptides isolated from the shrimp Penaeus vannamei (Decapoda). J Biol Chem 272:28398–28406PubMedCrossRefGoogle Scholar
  12. Destoumieux D, Muñoz M, Cosseau C, Rodriguez J, Bulet P, Comps M, Bachère E (2000) Penaeidins, antimicrobial peptides with chitin-binding activity, are produced and stored in shrimp granulocytes and released after microbial challenge. J Cell Sci 113:461–469PubMedGoogle Scholar
  13. Euzet L, Combes C (1980) Les problèmes de l’espèce chez les animaux parasites. In: Boquet C, Genermont J, Lamotte M (eds) Les problèmes de l’espèce dans le règne animal. Tome III. Mémoires de la Société Zoologique Française 40:239–285Google Scholar
  14. Fagutao FF, Koyama T, Kaizu A, Saito-Taki T, Kondo H, Aoki T, Hirono I (2009) Increased bacterial load in the shrimp hemolymph in the absence of prophenoloxidase. FEBS J 276:5298–5306PubMedCrossRefGoogle Scholar
  15. Fredensborg BL, Poulin R (2006) Parasitism shaping host life-history evolution: adaptive responses in a marine gastropod to infection by trematodes. J Anim Ecol 75:44–53PubMedCrossRefGoogle Scholar
  16. Fredensborg BL, Mouritsen KN, Poulin R (2004) Intensity-dependent mortality of Paracalliope novizealandiae (Amphipoda: Crustacea) infected by a trematode: experimental infections and field observations. J Exp Mar Biol Ecol 311:253–265CrossRefGoogle Scholar
  17. Galaktionov KV, Malkova II, Irwin SWB, Saville DH, Maguire JG (1996) Developmental changes in the tegument of four microphallid metacercariae in their second (crustacean) intermediate hosts. J Helminthol 70:201–210CrossRefGoogle Scholar
  18. Hose JE, Martin GG, Gerard AS (1990) A decapod hemocyte classification scheme integrating morphology, cytochemistry and function. Biol Bull 178:33–45CrossRefGoogle Scholar
  19. 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 33:1055–1063PubMedCrossRefGoogle Scholar
  20. Jiravanichpaisal P, Lee BL, Söderhäll K (2006) Cell-mediated immunity in arthropods: hematopoiesis, coagulation, melanisation and opsonization. Immunobiology 211:213–236PubMedCrossRefGoogle Scholar
  21. Keeney DB, Waters JM, Poulin R (2007) Diversity of trematode genetic clones within amphipods and the timing of same-clone infections. Int J Parasitol 37:351–357PubMedCrossRefGoogle Scholar
  22. Kitaura J, Wada K, Nishida M (2002) Molecular phylogeny of grapsoid and ocypodoid crabs with special reference to the genera Metaplax and Macrophthalmus. J Crustac Biol 22:682–693CrossRefGoogle Scholar
  23. Koehler AV, Poulin R (2010) Host partitioning by parasites in an intertidal crustacean community. J Parasitol 96:862–868PubMedCrossRefGoogle Scholar
  24. Kostadinova A, Mavrodieva RS (2005) Microphallids in Gammarus insensibilis Stock, 1966 from a Black Sea lagoon: host response to infection. Parasitology 131:347–354PubMedCrossRefGoogle Scholar
  25. Latham ADM, Poulin R (2002a) Effect of acanthocephalan parasites on hiding behaviour in two species of shore crabs. J Helminthol 76:323–326PubMedCrossRefGoogle Scholar
  26. Latham ADM, Poulin R (2002b) Field evidence of the impact of two acanthocephalan parasites on the mortality of three species of New Zealand shore crabs (Brachyura). Mar Biol 141:1131–1139CrossRefGoogle Scholar
  27. Liu H, Jiravanichpaisal P, Cerenius L, Lee BL, Söderhäll I, Söderhäll K (2007) Phenoloxidase is an important component of the defense against Aeromonas hydrophila infection in a crustacean, Pacifastacus leniusculus. J Biol Chem 282:33593–33598PubMedCrossRefGoogle Scholar
  28. Lochmiller RL, Deerenberg C (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88:87–98CrossRefGoogle Scholar
  29. Matozzo V, Marin MG (2010) The role of haemocytes from the crab Carcinus aestuarii (Crustacea, Decapoda) in immune responses: a first survey. Fish Shellfish Immunol 28:534–541PubMedCrossRefGoogle Scholar
  30. Moravec F, Fredensborg BL, Latham ADM, Poulin R (2003) Larval Spirurida (Nematoda) from the crab Macrophthalmus hirtipes in New Zealand. Folia Parasitol 50:109–114PubMedGoogle Scholar
  31. Perdomo-Morales R, Montero-Alejo V, Perera E, Pardo-Ruiz Z, Alonso-Jiménez E (2008) Hemocyanin-derived phenoloxidase activity in the spiny lobster Panulirus argus (Latreille, 1804). Biochim Biophys Acta 1780:652–658PubMedGoogle Scholar
  32. Poulin R, Mouritsen KN (2006) Climate change, parasitism and the structure of intertidal ecosystems. J Helminthol 80:183–191PubMedCrossRefGoogle Scholar
  33. Schmid-Hempel P (2003) Variation in immune defence as a question of evolutionary ecology. Proc R Soc Lond B 270:357–366CrossRefGoogle Scholar
  34. Schmid-Hempel P (2008) Parasite immune evasion: a momentous molecular war. Trends Ecol Evol 23:318–326PubMedCrossRefGoogle Scholar
  35. Schnapp D, Kemp GD, Smith VJ (1996) Purification and characterization of a proline-rich antibacterial peptide, with sequence similarity to bactenecin-7, from the haemocytes of the shore crab, Carcinus maenas. Eur J Biochem 240:532–539PubMedCrossRefGoogle Scholar
  36. Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321PubMedCrossRefGoogle Scholar
  37. Söderhäll K (1983) β-1,3 glucan enhancement of protease activity in crayfish hemocyte lysate. Comp Biochem Physiol B 74:221–224CrossRefGoogle Scholar
  38. Söderhäll K, Cerenius L (1998) Role of the prophenoloxidase-activating system in invertebrate immunity. Curr Opin Immunol 10:23–28PubMedCrossRefGoogle Scholar
  39. Thomas F, Renaud F, de Meeûs T, Poulin R (1998) Manipulation of host behaviour by parasites: ecosystem engineering in the intertidal zone? Proc R Soc B 265:1091–1096CrossRefGoogle Scholar
  40. Thomas F, Poulin R, de Meeüs T, Guégan J-F, Renaud F (1999) Parasites and ecosystem engineering: what roles could they play? Oikos 84:167–171CrossRefGoogle Scholar
  41. Thomas F, Guldner E, Renaud F (2000) Differential parasite (Trematoda) encapsulation in Gammarus aequicauda (Amphipoda). J Parasitol 86:650–654PubMedGoogle Scholar
  42. Vazquez L, Alpuche J, Maldonado G, Agundis C, Pereyra-Morales A, Zenteno E (2009) Immunity mechanisms in crustaceans. Innate Immun 15:179–188PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Jessica Dittmer
    • 1
    Email author
  • Anson V. Koehler
    • 2
  • Freddie-Jeanne Richard
    • 1
  • Robert Poulin
    • 2
  • Mathieu Sicard
    • 1
  1. 1.Laboratoire Ecologie, Evolution, Symbiose, UMR CNRS 6556Université de PoitiersPoitiersFrance
  2. 2.Department of ZoologyUniversity of OtagoDunedinNew Zealand

Personalised recommendations