Abstract
The intertidal cockle Austrovenus stutchburyi exists in a symbiotic relationship with the mud flat anemone Anthopleura aureoradiata, the latter using the shell of buried cockles as the only available hard substrate for attachment. The cockles are also host to a detrimental larval trematode Curtuteria australis that invades the bivalves through the filtration current, and here we demonstrate that the anemones significantly depress the rate by which cockles accumulate parasites in the field. Along the tidal gradient, the relative parasite load of cockles was lowest where anemones were most abundant, and the area occupied by anemones per square meter sediment surface explained 30% of the spatial variation in infection intensity. At a smaller spatial scale, parasite loads were significantly lower (34%) in cockles from patches with than without anemones at the same tidal height. A field experiment manipulating the density of anemones showed that the rate of parasite accumulation in cockles decreased with increasing anemone density, and that the generally positive relationship between infection intensity and cockle size tended to disappear in the presence of anemones. The results suggest that the anemone-cockle symbiosis is a non-obligate mutualistic relationship in which the former is provided with a suitable substrate for attachment whereas the latter obtains protection against parasitic infections.
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References
Acuna FH, Zamponi MO (1995) Feeding ecology of intertidal sea anemones (Cnidaria, Actiniaria): food sources and trophic parameters. Biociencias 3:73–84
Allison FR (1979) Life cycle of Curtuteria australis n. sp. (Digenea: Echinostomatidae: Himasthlinae), intestinal parasite of the South Island pied oystercatcher. NZ J Zool 6:13–20
Anderson RM, Gordon DM (1982) Processes influencing the distribution of parasite numbers within host populations with special emphasis on parasite-induced host mortalities. Parasitology 85:373–398
Anderson RM, Whitfield PJ, Dobson AP, Keymer AE (1978) Concomitant predation and infection processes: an experimental study. J Anim Ecol 47:891–911
Brooks WR (1988) The influence of the location and abundance of the sea anemone Calliactis tricolor (Le Sueur) in protecting hermit crabs from octopus predators. J Exp Mar Biol Ecol 116:15–21
Bunnag T, Rabelo de Freitas J, Scott HG (1977) The predatory activity of Lebistes reticulatus (Peters, 1859) on Schistosoma mansoni miracidia in laboratory experiments. Trop Geogr Med 29:411–414
Chintiroglou C, Koukouras A (1992) The feeding habits of three Mediterranean sea anemone species, Anemonia viridis (Forskaal), Actinia equina (Linnaeus) and Cereus pedunculatus (Pennant). Helgol Wiss Meeresunters 46:53–68
Christensen NO (1979) Schistosoma mansoni: interference with cercarial host-finding by various aquatic organisms. J Helminthol 53:7-14
Christensen NO, Frandsen F, Nansen P (1980) The interaction of some environmental factors influencing Schistosoma mansoni cercarial host-finding. J Helminthol 54:203–205
Côté IM (2000) Evolution and ecology of cleaning symbioses in the sea. Oceanogr Mar Biol 38:311–355
Fashuyi SA, Williams MO (1977) The role of Chaetogaster limnaei in the dynamics of trematode transmission in natural populations of freshwater snails. Z Parasitenkd 54:55–60
Fernandez J, Goater TM, Esch GW (1991) Population dynamics of Chaetogaster limnaei limnaei (Oligochaeta) as affected by a trematode parasite in Helisoma anceps (Gastropoda). Am Midl Nat 125:195–205
Hudson PJ, Rizzoli A, Grenfell BT, Heesterbeek H, Dobson AP (2002) The ecology of wildlife diseases. Oxford University Press, Oxford
Khalil LF (1961) On the capture and destruction of miracidia by Chaetogaster limnaei (Oligochaeta). J. Helminthol 35:269–274
Kearn GC (1998) Parasitism and the platyhelminths. Chapman and Hall, London
Kruger LM, Griffiths CL (1996) Sources of nutrition in intertidal sea anemones from the south-western Cape, South Africa. S Afr J Zool 31:110–119
Kruger LM, Griffiths CL (1998) Sea anemones as secondary consumers on rocky shores in the south-western Cape, South Africa. J Nat Hist 32:629–644
Montaudouin X de, Wegeberg AM, Jensen KT, Sauriau PG (1998) Infection characteristics of Himasthla elongata cercariae in cockles as a function of water current. Dis Aquat Org 34:63–70
Morton J, Miller M (1973) The New Zealand sea shore, 2nd edn. Collins, London
Mouritsen KN (2002) The parasite-induced surfacing behaviour in the cockle Austrovenus stutchburyi: a test of an alternative hypothesis and identification of potential mechanisms. Parasitology 124:521–528
Mouritsen KN, Poulin R (2002) The risk of being at the top: foot-cropping in the New Zealand cockle Austrovenus stutchburyi. J Mar Biol Assoc UK (in press)
Patzig F, Schmid K (1981) Chaetogaster limnaei K.E. v. Baer. Ein Problem in der Labor-wasserschneckenzucht für die Trematodenforschung. Z Parasitenkd 65:261–270
Poulin R, Grutter AS (1996) Cleaning symbioses: proximate and adaptive explanations. BioScience 46:512–517
Rajasekariah GR (1978) Chaetogaster limnaei K. von Baer 1872 on Lymnaea tomentosa: ingestion of Fasciola hepatica cercariae. Experientia 34:1458–1459
Shepherd SA, Gray JD (1986) Food of the anemone Anthothoe albocincta at West Island, South Australia. Trans R Soc S Aust 110:191–192
Stirewalt M, Lewis FA (1981) Schistosoma mansoni: effect of rotifers on cercarial output, motility and infectivity. Int J Parasitol 11: 301–303
Thomas F, Poulin R (1998) Manipulation of a mollusc by a trophically transmitted parasite: convergent evolution or phylogenetic inheritance? Parasitology 116:431–436
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 Lond B 265:1091–1096
Wajdi N (1964) The predation of Schistosoma mansoni by the oligochaete annelid Chaetogaster. J Helminthol 38:391–392
Wilson K, Bjørnstad ON, Dobson AP, Merler S, Poglayen G, Randolph SE, Read AF, Skorping A (2002) Heterogeneities in macroparasite infections: patterns and processes. In: Hudson PJ, Rizzoli A, Grenfell BT, Heesterbeek H, Dobson AP (eds) The ecology of wildlife diseases. Oxford University Press, Oxford, pp 6–44
Acknowledgements
The work was financially supported by the Marsden Fund, The Danish Natural Science Research Council (K.N.M), and via a James Cook Research Fellowship from the Royal Society of New Zealand (R.P.). We also wish to thank the referees for useful comments on an earlier draft.
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Mouritsen, K.N., Poulin, R. The mud flat anemone-cockle association: mutualism in the intertidal zone?. Oecologia 135, 131–137 (2003). https://doi.org/10.1007/s00442-003-1183-x
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DOI: https://doi.org/10.1007/s00442-003-1183-x