Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Spatial variation in parasite-induced mortality in an amphipod: shore height versus exposure history


Characterizing the causes of spatial and temporal variation in parasite-induced mortality under natural conditions is crucial to better understanding the factors driving host population dynamics. Our goal was to quantify this variation in the amphipod Paracalliope novizealandiae, a second intermediate host of the trematode, Maritrema novaezealandensis. If infection and development of trematode metacercariae are benign, we expected mature metacercariae to accumulate within amphipods inhabiting high infestation areas. In field samples, intensity levels of mature metacercariae decreased linearly when amphipods harbored >5 immature metacercariae. This finding is consistent with the hypothesis that the parasite can be detrimental at high intensities of infection. Short-term field experiments showed that host survival also declines with the intensity of new infections and drops below 80% when early stage metacercariae reach 10 amphipod−1. However, parasite effects varied over space and time. High-shore amphipods suffered an increased risk of infection in the summer and a lower likelihood of survival: there was a 10–30% decrease in survivorship for any given infection intensity at high- versus low-shore locations. We also tested for differences in the susceptibility of naive and exposed populations using transplant experiments, and found that naive amphipods acquired greater parasite loads (on average, 4.7 vs. 2.8 metacercariae amphipod−1). Because survival decreases rapidly with infection intensity of both early- and late-stage metacercariae, naive populations would suffer considerably if the parasite were to increase its range. Our results indicate that trematode infections cause high mortality in amphipods during summer months under natural conditions, and emphasize that the effects of parasitism vary at local spatial scales and with exposure history.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5


  1. Adler FR, Kretzschmar M (1992) Aggregation and stability in parasite-host models. Parasitology 104:199–205

  2. Anderson RM, May RM (1978) Regulation and stability of host-parasite population interactions, I: regulatory processes. J Anim Ecol 47:219–247

  3. Anderson RM, May RM (1982) Coevolution of hosts and parasites. Parasitology 85:411–426

  4. Bryan-Walker K, Leung TLF, Poulin R (2007) Local adaptation of immunity against a trematode parasite in marine amphipod populations. Mar Biol 152:687–695

  5. Cummings VJ, Pridmore RD, Thrush S, Hewitt JE (1995) Post-settlement movement by intertidal benthic macroinvertebrates: Do common New Zealand species drift in the water column? NZ J Mar Freshw Res 29:59–67

  6. Ewald PW (1983) Host-parasite relations, vectors, and the evolution of disease severity. Annu Rev Ecol Sys 14:465–485

  7. Fleischer J, Grell M, Hoeg JT, Olesen J (1992) Morphology of grooming limbs in species of Petrolisthes and Pachycheles (Crustacea: Decapoda: Anomura: Porcellanidae): a scanning electron microscopy study. Mar Biol 113:425–435

  8. 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 311:253–265

  9. Harvell CD, Kim K, Burkholder JM, Colwell RR, Epstein PR, Grimes DJ, Hofmann EE, Lip EK, Osterhaus ADME, Overstreet RM, Porter JW, Smith GW, Vasta GR (1999) Emerging marine diseases-climate links and anthropogenic factors. Science 285:1505–1510

  10. Hasu T, Benesh DP, Valtonen (2009) Differences in parasite susceptibility and costs of resistance between naturally exposed and unexposed host populations. J Evol Biol 22:699–707

  11. Hudson PJ, Dobson AP, Newborn D (1998) Prevention of population cycles by parasite removal. Science 282:2256

  12. Jensen KT, Mouritsen KN (1992) Mass mortality in two common soft-bottom invertebrates, Hydrobia ulvae and Corophium volutator-the possible role of trematodes. Helgol Meeresunters 46:329–339

  13. Jensen T, Jensen KT, Mouritsen KN (1998) The influence of the trematode Microphallus claviformis on two congeneric intermediate host species (Corophium): infection characteristics and host survival. J Exp Mar Biol Ecol 227:35–48

  14. Keeney DB, Waters JM, Poulin R (2007) Diversity of trematode genetic clones within amphipods and the timing of same-clone infections. Int J Parasitol 37:351–357

  15. Leung TLF, Poulin R (2006) Effects of the trematode Maritrema novaezealandensis on the behaviour of its amphipod host: adaptive or not? J Helminthol 80:271–275

  16. Lohse K, Gutierrez A, Kaltz O (2006) Experimental evolution of resistance in Paramecium caudatum against the bacterial parasite Holospora undulate. Evolution 60(6):1177–1186

  17. Martorelli SR, Fredensborg BL, Mouritsen KN, Poulin R (2004) Description and proposed life cycle of Maritrema novaezealandensis n. sp. (Microphallidae) parasitic in red-billed gulls, Larus novaehollandiae scopulinus, from Otago Harbor, South Island, New Zealand. J Parasitol 90(2):272–277

  18. May RM, Anderson RM (1978) Regulation and stability of host-parasite population interactions II. Destabilizing processes. J Anim Ecol 47:249–267

  19. May RM, Anderson RM (1983) Epidemiology and genetics in the coevolution of parasites and hosts. Proc R Soc Lond B 219:281–313

  20. Meißner K, Bick A (1999) Mortality of Corophium volutator (Amphipoda) caused by infestation with Maritrema subdolum (Digenea, Microphallidae)-laboratory studies. Dis Aquat Org 35:47–52

  21. Meißner K, Schaarschmidt T (2000) Ecophysiological studies of Corophium volutator (Amphipoda) infested by microphallid trematodes. Mar Ecol Prog Ser 202:143–151

  22. Meyers TR (1990) Diseases of Crustacea. Diseases caused by protistans and metazoans. In: Kinne O (ed) Diseases of Marine Animals. Volume III: Introduction, Cephalopoda, Annelida, Crustacea, Chaetognatha, Echinodermata, Urochordata. Biologische Anstalt Helgoland, Hamburg, pp 350–423

  23. Moret Y, Schmid-Hempel P (2000) Survival for immunity: the price of immune system activation for bumblebee workers. Science 290:1166–1168

  24. Mouritsen KN (2002) The Hydrobia ulvaeMaritrema subdolum association: influence of temperature, salinity, light, water-pressure and secondary host exudates on cercarial emergence and longevity. J Helminthol 76:341–347

  25. Mouritsen KN, Jensen KT (1997) Parasite transmission between soft-bottom invertebrates: temperature mediated infection rates and mortality in Corophium volutator. Mar Ecol Prog Ser 151:123–134

  26. Mouritsen KN, Poulin R (2003) The mud flat anemone-cockle association: mutualism in the intertidal zone? Oecologia 135:131–137

  27. Mouritsen KN, Tompkins DM, Poulin R (2005) Climate warming may cause a parasite induced collapse in coastal amphipod populations. Oecologia 146:476–483

  28. Poulin R (2006) Global warming and temperature-mediated increases in cercarial emergence in trematode parasites. Parasitology 132:143–151

  29. Poulin R, Latham ADM (2003) Effects of initial (larval) size and host body temperature on growth in trematodes. Can J Zool 81:574–581

  30. Raffaelli DG, Hawkins SJ (1996) Intertidal Ecology. Chapman and Hall, London

  31. Rigby MC, Hechinger RF, Stevens L (2002) Why should parasite resistance be costly? Trends Parasitol 18:116–120

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

  33. Thieltges DW, Jensen KT, Poulin R (2008) The role of biotic factors in the transmission of free-living endohelminth stages. Parasitology 135:407–426

  34. Thieltges DW, Fredensborg BL, Poulin R (2009) Geographical variation in metacercarial infection levels in marine invertebrate hosts: parasite species character versus local factors. Mar Biol 156:983–990

  35. Thomas F, Villa M, Montoliu I, Santalla F, Ce′zilly F, Renaud F (1998) Analyses of a debilitating parasite (Microphallus papillorobustus, Trematoda) and its ‘‘hitchhiker’’ parasite (Maritrema subdolum, Trematoda) on survival of their intermediate host (Gammarus insensibilis, Amphipoda). J Helminthol Soc Wash 65:1–5

  36. Tompkins DM, Begon M (1999) Parasites can regulate wildlife populations. Parasitol Tod 15:311–313

  37. Tompkins DM, Dobson AP, Arneberg P, Begon ME, Cattadori IM, Greenman JV, Heesterbeek JAP, Hudson PJ, Newborn D, Pugliese J, Rizzoli AP, Rosà R, Rosso F, Wilson K (2002) Parasites and host population dynamics. In: Hudson PJ, Dobson AP (eds) Ecology of wildlife diseases. Oxford University Press, New York, pp 45–62

  38. Webster JP, Gower CM, Blair L (2004) Do hosts and parasites coevolve? Empirical support from the Schistosoma system. Am Nat 164:S33–S51

Download references


Logistical assistance from the Portobello Marine Laboratory staff, in particular B. Dickson, is greatly appreciated. We also thank A. Koehler, T. Leung and A. Studer for expertise during the planning stages of this project. Financial support was provided by the University of Otago and a post-doctoral fellowship to A. Bates by the National Sciences and Engineering Research Council of Canada.

Author information

Correspondence to A. E. Bates.

Additional information

Communicated by Steven Kohler.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 76 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Bates, A.E., Poulin, R. & Lamare, M.D. Spatial variation in parasite-induced mortality in an amphipod: shore height versus exposure history. Oecologia 163, 651–659 (2010). https://doi.org/10.1007/s00442-010-1593-5

Download citation


  • Paracalliope novizealandiae
  • Maritrema novaezealandensis
  • Microphallidae
  • Parasite
  • Susceptibility
  • Naive host