Parasite-modified behaviour in non-trophic transmission: trematode parasitism increases the attraction between snail intermediate hosts

Abstract

J.T. Detwiler). Parasite-modified behaviour in non-trophic transmission: Trematode parasitism increases the attraction between snail intermediate hosts Many parasites with complex life cycles cause host behavioral changes that increase the likelihood of transmission to the next host. Parasite modification is often found in trophic transmission, but its influence on non-trophic transmission is unclear. In trematodes, transmission from the first to second intermediate host is non-trophic suggesting that free-swimming larvae (cercariae) emerging in closer proximity to the next host would have higher transmission success. We performed a series of behavioral experiments with echinostome trematodes and their snail hosts to determine if potential second hosts (Planorbella sp.) were more attracted to parasitized first hosts (Lymnaea elodes Say, 1821). In a Y-maze, a responding snail (Planorbella Haldeman, 1842 sp.) was placed in the base and its response to five treatments was assessed: no stimulus, duckweed (a food item, Lemna turionifera Landolt), non-parasitized L. elodes, parasitized L. elodes, and finally parasitized versus non-parasitized L. elodes. Snails showed some attraction to uninfected snails, but had a stronger response to infected first host snails. These results indicate that potential second host snails were more attracted to parasitized, heterospecific first host snails over non-parasitized heterospecific snails. This study demonstrates that echinostome trematodes alter snail behaviour by changing navigational choices in uninfected potential hosts through a chemical communication mechanism. Many trematode species cause behavioural changes in their intermediate hosts, which makes the transmission of the larval parasites to the next host more likely (Moore 1984; Cézilly et al. 2010; Lafferty and Shaw 2013). Most studies of trematode-altered behaviour have demonstrated its importance in trophic transmission whereby second intermediate hosts are consumed by definitive hosts (Lafferty and Shaw 2013). In these cases, second intermediate hosts, infected with encysted parasites (metacercariae), behavein ways that make predation and thus consumption of parasites by the next host in the life cycle more likely. For example, brain-encysting metacercariae cause ants to change their activity and microhabitat choice by freezing on the top of a blade of grass, making predation by grazing ungulate hosts more likely (Moore 1984). Likewise, fish infected with metacercariae behaved more conspicuously and were more likely to be eaten by bird hosts (Lafferty and Morris 1996). ). We used parasitized L. elodes as first intermediate hosts, and non-parasitized Planorbella sp. snails as potential second intermediate hosts to test whether parasitemodified behaviour affected heterospecific snail interactions. We hypothesized that if parasites modify host interactions, then uninfected Planorbella sp. snails would be more attracted to parasitized L. elodes first intermediate host snails compared to uninfected L. elodes.

Freshwater disease hotspots: Drivers of fine‐scale spatial heterogeneity in trematode parasitism in streams

“…Leaf litter patches are often colonised by many other macroinvertebrates that also consume leaves such as caddisflies, stoneflies, and crayfish (Leroy & Marks, 2006; Motomori et al., 2001), which can be second intermediate hosts for some of trematode taxa found in Juga (e.g., Microphalloidea; Burns, 1961). This aggregation of Juga with multiple downstream hosts residing in the same leaf patch might enhance transmission success, especially if cercariae shed from snails have an increased likelihood of infecting secondary hosts in close proximity (Eliuk et al., 2020; Gray et al., 2009). Leaf litter may also serve as a refuge for the trematode transmission stages (i.e., miracidia, cercariae), but we are not aware of any studies supporting this idea.…”

Density-Dependent Prophylaxis in Freshwater Snails Driven by Oxylipin Chemical Cues

“…We sequenced the DNA at the NADH dehydrogenase 1 (ND1) gene and compared our sequences to ones published on GenBank and our own database to identify the parasites as Echinoparyphium sp. lineage 2 ( 71 ). Each sample was prepared and analysed as described in detail in Eliuk et al., 2020 ( 71 ).…”

“…lineage 2 ( 71 ). Each sample was prepared and analysed as described in detail in Eliuk et al., 2020 ( 71 ).…”

Effects of larval trematode parasitism on the reproductive capacity of Manila clam Ruditapes philippinarum in a sandy-mud tidal flat on the west coast of Korea

“…The digeneans in a sporocyst stage generally utilize mollusks as the first intermediate host and invade a variety of vertebrates and invertebrates in the form of metacercaria (Littlewood, 2006). The metacercaria infection often results in retarded growth (Wegeberg and Jensen, 2003;Thieltges, 2006a); increased energy demand (Magalhães et al, 2019); manipulation of host behavior, leading the host to become conspicuous to their predators (Lafferty and Morris, 1996;Thomas and Poulin, 1998;Eliuk et al, 2020); and mortalities (Gordon and Rau, 1982;Jacobson et al, 2008;Magalhães et al, 2015). However, most metacercaria infections pose a relatively minor impact on hosts, as they do not reproduce in the host (Bower et al, 1994;Rhode, 2005).…”