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.

Chemosensory behaviors of parasites

“…After 1–3 hours, miracidia exhibit short-range host-seeking behaviors and are capable of responding to snail-secreted chemicals [49]. Response to snail-derived odor clouds increases miracidial transmission success, confirming an important role for chemosensation in the host infection process [50]. The snail-derived cues that attract miracidia are not fully understood but are thought to include amino acids, fatty acids, ammonia, and a number of different glycoproteins [49].…”

Snails, waterfowl and cercarial dermatitis

“…(2005)) are able to distinguish snail species from a distance, recognising clouds of molecules (e.g., glycoproteins called miraxons or MAGs = miracidia‐attracting glycoproteins) emitted by the snails. It is hypothesised that these molecules are pheromones that are essential for intraspecific communication within snail populations and that miracidia incidentally use these molecules to identify hosts (Haas, 2003; Hertel et al. , 2006).…”

Larval trematodes in freshwater molluscs from the Elbe to Danube rivers (Southeast Germany): before and today

“…Nowadays, the occurrence of trematode larvae is not observed and only selected species, such as those of Echinostoma, Echinoparyphium, and Trichobilharzia, are used as model organisms for physiological and behavioral investigations and studies on parasite-host relationships Haas 2003;Hertel et al 2006). Attention is also currently given to surveys of cercariae from the family Schistosomatidae (genus Trichobilharzia), the causative agents of cercarial dermatitis, as an emerging disease in South Germany (Allgöwer 1990(Allgöwer , 1995Allgöwer and Matuschka 1993;Pilz et al 1995).…”