Snail odour-clouds: spreading and contribution to the transmission success of Trichobilharzia ocellata (Trematoda, Digenea) miracidia
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Chemical communication among freshwater organisms is an adaptation to improve their coexistence. Here,we focus on the chemical cues secreted by the freshwater gastropod Lymnaea stagnalis, which are known to stimulate behavioural responses of Trichobilharzia ocellata (Plathelminthes, Digenea, Trematoda) miracidia. Such responses are commonly claimed to influence transmission positively, but in response to chemical cues miracidia randomly change their swimming direction. This kind of response does not necessarily increase transmission, because miracidia may be trapped at the periphery of very large snail odour-clouds, which may prevent them from approaching the snail. On the other hand, the odour clouds may be too small to improve host-localisation. To shed light on these scenarios, the spreading of molecules released around L. stagnalis (active space) was visualised by recording host-finding responses of T. ocellata miracidia when they approached snails. Behavioural responses of miracidia indicated the spreading of compounds forming an attractive active space only around the host-snail L. stagnalis, but not around sympatric non-host-snail species. The active space increased approximately linearly with the time the snail rested at the same spot and within 5 min it reached a volume of more than 30 times that of the snail. We also demonstrated in a large-scale experiment, that the active space of L. stagnalis significantly increases the transmission success of T. ocellata miracidia. Additionally, the microhabitat selection of T. ocellata miracidia was studied, demonstrating that peripheral locations near the water surface were preferred, which are also preferred sites of L. stagnalis. Improved chemoperception and microhabitat selection may have been a consequence of coevolution with snails and benefited miracidia, which became efficient transmissive stages.
KeywordsBehavioural ecology Chemical ecology Host-finding Lymnaea Microhabitat selection
We are indebted to 2 unknown reviewers for their excellent revision, which significantly contributed to improve the manuscript. We thank Christina Loy for technical assistance in development and improvement of the miracidia sampling technique. We also thank Susanne Steineke for pioneer work on larval sampling procedures. This work was financed by the Deutsche Forschungsgemeinschaft and the work complies with the current law of Germany.
- Combes C, Bartoli P, Theron A (2002) Trematode transmission strategies. In: Lewis EE, Campbell JF, Sukhdeo MVK (eds) Behavioural ecology of parasites. CABI Publishing, Wallingford, pp 1–12Google Scholar
- Haas W, Haberl B (1997) Host recognition by trematode miracidia and cercariae. In: Fried B, Graczyk TK (eds) Advances in trematode biology. CRC Press, Boca Raton, pp 197–227Google Scholar
- Painter SD, Cummins SF, Nichols AE, Akalal DBG, Schein CH, Braun W, Smith JS, Susswein AJ, Levy M, de Boer PAC, ter Maat A, Miller MW, Scanlan C, Milberg RM, Sweedler JV, Nagle GT (2004) Structural and functional analysis of Aplysia attractins, a family of water-borne protein pheromones with interspecific attractiveness. Proc Natl Acad Sci U S A 101:6929–6933PubMedCrossRefGoogle Scholar
- Rittschof D (1993) Body odour and neutral-basic peptide mimics: a review of responses by marine organisms. Am Zool 33:487–493Google Scholar
- Sapp KK, Loker ES (2002) A comparative study of mechanisms underlying digenean-snail specificity: in vitro interactions between hemocytes and digenean larvae. J Parasitol 86:1020–1029Google Scholar
- Takahashi T, Mori K, Shigeta Y (1961) Phototactic, thermotactic and geotactic responses of miracidia of Schistosoma japonicum. Jpn J Parasitol 10:686–691Google Scholar
- Thomas JD, Eaton P (1993) Amino acid medleys of snail origin as possible sources of information for conspecifics, schistosome miracidia and predators. Comp Biochem Physiol C 106:781–796Google Scholar