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Parasitology Research

, Volume 101, Issue 2, pp 281–287 | Cite as

Recruitment rate of gymnophallid metacercariae in the New Zealand cockle Austrovenus stutchburyi: an experimental test of the hitch-hiking hypothesis

  • Tommy L. F. LeungEmail author
  • Robert Poulin
Original Paper

Abstract

The rate at which host organisms accumulate parasites is affected by a number of intrinsic and extrinsic factors. The New Zealand cockle Austrovenus stutchburyi is frequently parasitised by trematodes comprising of two species of echinostomes and a species of gymnophallid that use it as a second intermediate host for trophic transmission to avian definitive hosts. The echinostomes are capable of manipulating the burrowing behaviour of the cockle to enhance their transmission success, whereas the gymnophallid is not capable of host manipulation. Previous studies have found patterns of positive associations between the echinostomes and the gymnophallid. Thus, it is possible that the latter is a “hitch-hiking” parasite that preferentially infects cockles already heavily infected by echinostome metacercariae to enhance its own transmission rate. A field experiment involving cockles forced to remain either above or below the sediment surface to simulate manipulated and non-manipulated cockles was conducted to test the hitch-hiking hypothesis. The gymnophallid was not found to display any preference for either surfaced or buried cockles; therefore, it cannot be considered as a hitch-hiking parasite. Possible alternative reasons for the pattern of positive association between the gymnophallid and the echinostomes are proposed.

Keywords

Intermediate Host Definitive Host Burial Depth Infection Intensity Baseline Group 
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.

Notes

Acknowledgements

The authors would like to thank Florian Weller for providing assistance with setting up the field experiment and Clément Lagrue and Kim Bryan-Walker for help with the maintenance of the cockle cages. The experiments conducted for this study comply with the current laws of New Zealand.

References

  1. Ansell AD (2001) Dynamics of aggregations of a gastropod predator/scavenger on a New Zealand harbour beach. J Molluscan Stud 67:329–341CrossRefGoogle Scholar
  2. Babirat C, Mouritsen KN, Poulin R (2004) Equal partnership: two trematode species, not one, manipulate the burrowing behaviour of the New Zealand cockle, Austrovenus stutchburyi. J Helminthol 78:195–199PubMedCrossRefGoogle Scholar
  3. Blundon JA, Kennedy VS (1982) Refuges for infaunal bivalves from blue crab, Callinectes sapidus (Rathbun), predation in Chesapeake Bay. J Exp Mar Biol Ecol 76:201–223Google Scholar
  4. Bower EA, Bartoli P, Russell-Pinto F, James, BL (1996) The metacercariae of sibling species of Meiogymnophallus, including M. rebecqui comb. nov. (Digenea: Gymnophallidae), and their effects on closely related Cerastoderma host species (Mollusca: Bivalvia). Parasitol Res 82:505–510CrossRefGoogle Scholar
  5. Buck BH, Thieltges DW, Walter U, Nehls G, Rosenthal H (2005) Inshore–offshore comparison of parasite infestation in Mytilus edulis: implications for open ocean aquaculture. J Appl Ichthyol 21:107–113CrossRefGoogle Scholar
  6. de Goeij P, Luttikhuizen PC (1998) Deep-burying reduces growth in intertidal bivalves: field and mesocosm experiments with Macoma balthica. J Exp Mar Biol Ecol 228:327–337CrossRefGoogle Scholar
  7. de Goeij P, Honkoop PJC (2003) Experimental effects of immersion time and water temperature on body condition, burying depth and timing of spawning of the tellinid bivalve, Macoma balthica. Helgoland Mar Res 57:20–26Google Scholar
  8. de Goeij P, Luttikhuizen PC, van der Meer J, Piersma T (2001) Facilitation on an intertidal mudflat: the effect of siphon nipping by flatfish on burying depth of the bivalve Macoma balthica. Oecologia 126:500–506CrossRefGoogle Scholar
  9. Desclaux C, de Montaudouin X, Bachelet G (2004) Cockle Cerastoderma edule population mortality: role of the digenean parasite Himasthla quissetensis. Mar Ecol Prog Ser 74:141–150CrossRefGoogle Scholar
  10. El-Darsh HEM, Whitfield PJ (1999) Digenean metacercariae (Timonella spp., Labratrema minimus and Cryptocotyle concava) from the flounder, Platichthys flesus, in the tidal Thames. J Helminthol 73:103–113Google Scholar
  11. Ferreira SM, Jensen KT, Pardal MA (2005) Infection characteristics of a trematode in an estuarine isopod: influence of substratum. Hydrobiologia 539:149–155CrossRefGoogle Scholar
  12. Grosholz ED (1994) The effects of host genotype and spatial distribution on trematode parasitism in a bivalve population. Evolution 48:1514–1524CrossRefGoogle Scholar
  13. Gurski KC, Ebbert MA (2003) Host age, but not host location within a stream, is correlated with the prevalence of gut parasites in water striders. J Parasitol 89:529–534PubMedCrossRefGoogle Scholar
  14. Helluy S (1983) Relations hôtes–parasites du trématode Microphallus papillorobustus (Rankin 1940). II Modifications du comportement des Gammarus hôtes intermédiaires et localisation des métacercaires. Ann Parasitol Hum Comp 58:1–17PubMedGoogle Scholar
  15. Jensen KT, Castro NF, Bachelet G (1999) Infectivity of Himasthla spp. (Trematoda) in cockle (Cerastoderma edule) spat. J Mar Biol Assoc UK 79:265–271CrossRefGoogle Scholar
  16. Jensen KT, Ferreira SM, Pardal MA (2004) Trematodes in a Cyathura carinata population from temperate intertidal estuary: infection patterns and impact on host. J Mar Biol Assoc UK 84:1151–1158CrossRefGoogle Scholar
  17. Karvonen A, Seppälä O, Valtonen ET (2004) Parasite resistance and avoidance behaviour in preventing eye fluke infections in fish. Parasitology 129:159–164PubMedCrossRefGoogle Scholar
  18. Kurihara T (2003) Adaptations of subtropical Venus clams to predation and desiccation: endurance of Gafrarium tumidum and avoidance of Ruditapes variegates. Mar Biol 143:1117–1125CrossRefGoogle Scholar
  19. Lafferty KD (1999) The evolution of trophic transmission. Parasitol Today 15:111–115PubMedCrossRefGoogle Scholar
  20. Lardies MA, Clasing E, Navarro JM, Stead RA (2001) Effects of environmental variables on burial depth of two infaunal bivalves inhabiting a tidal flat in southern Chile. J Mar Biol Assoc UK 81:809–816CrossRefGoogle Scholar
  21. Leung TLF, Poulin R (2007) Interactions between parasites of the cockle Austrovenus stutchburyi: Hitch-hikers, resident-cleaners, and habitat-facilitators. Parasitology 134(Pt 2):247–255PubMedCrossRefGoogle Scholar
  22. Mouritsen KN (2002) The parasite-induced surfacing behaviour in the cockle Austrovenus stutchburyi: a test of an alternative hypothesis and identification of potential mechanism. Parasitology 124:521–528PubMedCrossRefGoogle Scholar
  23. Mouritsen KN, Poulin R (2003) The mud flat anemone–cockle association: mutualism in the intertidal zone? Oecologia 135:131–137PubMedGoogle Scholar
  24. Ponton F, Biron DG, Joly C, Helluy S, Duneau D, Thomas F (2005) Ecology of parasitically modified populations: a case study from a gammarid–trematode system. Mar Ecol Prog Ser 299:205–215CrossRefGoogle Scholar
  25. Poulin R (1998) Evolutionary ecology of parasites: From individuals to communities. Chapman & Hall, LondonGoogle Scholar
  26. Poulin R (2001) Interactions between species and the structure of helminth communities. Parasitology 122:S3–S11PubMedCrossRefGoogle Scholar
  27. Poulin R, Fitzgerald GJ (1989) Risk of parasitism and microhabitat selection in juvenile sticklebacks. Can J Zool 67:14–18CrossRefGoogle Scholar
  28. Poulin R, Mouritsen KN (2004) Small-scale spatial variation in rates of metacercarial accumulation by a bivalve second intermediate host. J Mar Biol Assoc UK 84:1209–1212CrossRefGoogle Scholar
  29. Poulin R, Hecker K, Thomas F (1998) Hosts manipulated by one parasite incur additional costs from infection by another parasite. J Parasitol 84:1050–1052PubMedCrossRefGoogle Scholar
  30. Poulin R, Steeper MJ, Miller AA (2000) Non-random patterns of host use by the different parasite species exploiting a cockle population. Parasitology 121:289–295PubMedCrossRefGoogle Scholar
  31. Schmid-Hempel P (2003) Variation in immune defence as a question of evolutionary ecology. Proc R Soc Lond B Biol Sci 270:357–366CrossRefGoogle Scholar
  32. Thomas F, Poulin R (1998) Manipulation of a mollusc by a trophically transmitted parasite: convergent evolution or phylogenetic inheritance? Parasitology 116:431–436PubMedCrossRefGoogle Scholar
  33. Thomas F, Mete K, Helluy S, Santalla F, Verneau O, de Meeüs T, Cézilly F, Renaud F (1997) Hitch-hiker parasites or how to benefit from the strategy of another parasite. Evolution 51:1316–1318CrossRefGoogle Scholar
  34. Thomas F, Renaud F, Poulin R (1998a) Exploitation of manipulators: ‘hitch-hiking’ as a parasite transmission strategy. Anim Behav 56:199–206PubMedCrossRefGoogle Scholar
  35. Thomas F, Renaud F, Poulin R (1998b) Nonmanipulative parasites in manipulated hosts: ‘hitch-hikers’ or simply ‘lucky passengers’? J Parasitol 84:1059–1061PubMedCrossRefGoogle Scholar
  36. Timi JT, Lanfranchi AL (2006) Size relationships between the parasitic copepod, Lernanthropus cynoscicola, and its fish host, Cynoscion guatucupa. Parasitology 132:207–213PubMedCrossRefGoogle Scholar
  37. Tompkins DM, Mouritsen KN, Poulin R (2004) Parasite-induced surfacing in the cockle Austrovenus stuchburyi: adaptation or not? J Evol Biol 17:247–256PubMedCrossRefGoogle Scholar
  38. Webber RA, Rau ME, Lewis DJ (1989) The effects of host distributional patterns on parasite transmission: Aedes aegypti larvae and Plagiorchis noblei cercariae. J Parasitol 75:810–812PubMedCrossRefGoogle Scholar
  39. Wegeberg AM, Jensen KT (1999) Reduced survivorship of Himasthla (Trematoda: Digenea)-infected cockles (Cerastoderma edule) exposed to oxygen depletion. J Sea Res 42:325–331CrossRefGoogle Scholar
  40. Wegeberg AM, Jensen KT (2003) In situ growth of juvenile cockles, Cerastoderma edule, experimentally infected with larval trematodes (Himasthla interrupta). J Sea Res 50:37–43CrossRefGoogle Scholar
  41. Wegeberg AM, de Montaudouin X, Jensen KT (1999) Effect of intermediate host size (Cerastoderma edule) on infectivity of cercariae of three Himasthla species (Echinostomatidae, Trematoda). J Exp Mar Biol Ecol 238:259–269CrossRefGoogle Scholar
  42. Zaklan SD, Ydenberg R (1997) The body size–burial depth relationship in the infaunal clam Mya arenaria. J Exp Mar Biol Ecol 215:1–17CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  1. 1.Department of ZoologyUniversity of OtagoDunedinNew Zealand

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