Advertisement

Snail odour-clouds: spreading and contribution to the transmission success of Trichobilharzia ocellata (Trematoda, Digenea) miracidia

Abstract

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.

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

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 199

This is the net price. Taxes to be calculated in checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Reference

  1. Basch PF (1976) Intermediate host specificity in Schistosoma mansoni. Exp Parasitol 39:150–169

  2. Brönmark C, Hansson LA (2000) Chemical communication in aquatic systems. Oikos 88:103–109

  3. Burks RL, Lodge DM (2002) Cued in: advances and opportunities in freshwater chemical ecology. J Chem Ecol 28:1901–1917

  4. Chernin E, Dunavan CA (1962) The influence of host–parasite dispersion upon the capacity of Schistosoma mansoni miracida to infect Australorbis glabratus. Am J Trop Med Hyg 11:455–471

  5. Christensen NO (1980a) A review of the influence of host- and parasite-related factors and environmental conditions on the host-finding capacity of the trematode miracidium. Acta Trop 37:303–318

  6. Christensen NO (1980b) Echinostoma revolutum: labelling of miracidia with radioselenium in vivo and assay for host-finding. Exp Parasitol 50:67–73

  7. 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 1–12

  8. Cummins SF, Nichols AE, Amare A, Hummon AB, Sweedler JV, Nagle GT (2004) Characterization of Aplysia Enectin and Temptin, two novel water-borne protein pheromones that act in concert with attractin to stimulate mate attraction. J Biol Chem 279:25614–25622

  9. Cummins SF, Nichols AE, Warso CJ, Nagle GT (2005) Aplysia seductin is a water-borne protein pheromone that acts in concert with attractin to stimulate mate attraction. Peptides 26:351–359

  10. Haas W (2003) Strategies for host-finding, recognition and invasion. Zoology 106:349–364

  11. 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 197–227

  12. Haberl B, Körner M, Spengler Y, Hertel J, Kalbe M, Haas W (2000) Host-finding in Echinostoma caproni: miracidia and cercariae use different signals to identify the same snail species. Parasitology 120:479–486

  13. Hassan AHM, Haberl B, Hertel J, Haas W (2003) Miracidia of an Egyptian strain of Schistosoma mansoni differentiate between sympatric snail species. J Parasitol 89:1248–1250

  14. Hertel J, Hamburger J, Haberl B, Haas W (2002) Detection of bird schistosomes in lakes by PCR and filter-hybridization. Exp Parasitol 101:57–63

  15. Hertel J, Haberl B, Hamburger J, Haas W (2003) Description of a tandem repeated DNA sequence of Echinostoma caproni and methods for its detection in snail and plankton samples. Parasitology 126:443–449

  16. Horak P, Kolarova L, Adema C (2002) Biology of the schistosome genus Trichobilharzia. Adv Parasitol 52:155–233

  17. Kalbe M, Haberl B, Haas W (1997) Miracidial host-finding in Fasciola hepatica and Trichobilharzia ocellata is stimulated by species-specific glycoconjugates from the host-snail. Parasitol Res 83:806–812

  18. Kalbe M, Haberl B, Haas W (2000) Finding of the snail host by Fasciola hepatica and Trichobilharzia ocellata: compound analysis of ‘Miracidia attracting glycoprotein’. Exp Parasitol 96:231–242

  19. Kalbe M, Haberl B, Hertel J, Haas W (2004) Heredity of specific host-finding behaviour in Schistosoma mansoni miracidia. Parasitology 128:635–643

  20. Kock S (2001) Investigations on intermediate host specificity help to elucidate the taxonomic status of Trichobilharzia ocellata (Digenea: Schistosomatidae). Parasitology 123:67–70

  21. Leduc AOH, Kelly JM, Brown GE (2004) Detection of conspecific alarm cues by juvenile salmonids under neutral and weakly acidic conditions: laboratory and field tests. Oecologia 139:318–324

  22. MacInnis AJ (1965) Responses of Schistosoma mansoni miracidia to chemical attractants. J Parasitol 51:731–746

  23. Moomjian L, Nystrom S, Rittschof D (2003) Behavioral responses of sexually active mud snails: kairomones and pheromones. J Chem Ecol 29:497–501

  24. 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 101:6929–6933

  25. Rea JG, Irwin SWB (1994) The ecology of host-finding behaviour and parasite transmission: past and future perspectives. Parasitology 109:S31–S39

  26. Rittschof D (1993) Body odour and neutral-basic peptide mimics: a review of responses by marine organisms. Am Zool 33:487–493

  27. Rudolfova J, Hampl V, Bayssade-Dufour C, Lockyer AE, Littlewood DTJ, Horak P (2005) Validity reassessment of Trichobilharzia species using Lymnaea stagnalis as the intermediate host. Parasitol Res 95:79–89

  28. Saladin KS (1979) Behavioral parasitology and perspectives on miracidial host-finding. Z Parasitenkd 60:197–210

  29. Sapp KK, Loker ES (2002) A comparative study of mechanisms underlying digenean-snail specificity: in vitro interactions between hemocytes and digenean larvae. J Parasitol 86:1020–1029

  30. Sukhdeo MVK, Sukhdeo SC (2004) Trematode behaviours and the perceptual worlds of parasites. Can J Zool 82:292–315

  31. Susswein AJ, Nagle GT (2004) Pepetide and protein pheromones in molluscs. Peptides 25:1523–1530

  32. Takahashi T, Mori K, Shigeta Y (1961) Phototactic, thermotactic and geotactic responses of miracidia of Schistosoma japonicum. Jpn J Parasitol 10:686–691

  33. Theron A, Sire C, Rognon A, Prugnolle F, Durand P (2004) Molecular ecology of Schistosoma mansoni transmission inferred from the genetic composition of larval and adult infrapopulations within intermediate and definitive hosts. Parasitology 129:571–585

  34. 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 106:781–796

  35. Upatham ES (1972) Exposure of caged Biomphalaria glabrata to investigate dispersion of miracidia of Schistosoma mansoni in field simulated and field habitats in St Lucia, West Indies. J Helminthol 46:297–306

  36. Webster JP, Hoffman JI, Berdoy M (2003) Parasite infection, host resistance and mate choice: battle of the genders in a simultaneous hermaphrodite. Proc R Soc Lond B 270:1481–1485

  37. Winnepenninckx B, Backeljau T, De Wachter R (1993) Extraction of high molecular weight DNA from molluscs. Trends Genet 9:407

  38. Zhang SM, Adema CM, Kepler TB, Loker ES (2004) Diversification of Ig superfamily genes in an invertebrate. Science 305:251–254

Download references

Acknowledgement

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.

Author information

Correspondence to Jan Hertel.

Additional information

Communicated by Thomas Hoffmeister

Electronic supplementary material

Supplementary material

Supplementary material

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Hertel, J., Holweg, A., Haberl, B. et al. Snail odour-clouds: spreading and contribution to the transmission success of Trichobilharzia ocellata (Trematoda, Digenea) miracidia. Oecologia 147, 173–180 (2006) doi:10.1007/s00442-005-0239-5

Download citation

Keywords

  • Behavioural ecology
  • Chemical ecology
  • Host-finding
  • Lymnaea
  • Microhabitat selection