How cunning is the puppet-master? Cestode-infected fish appear generally fearless

Abstract

Trophically transmitted parasites have life cycles that require the infected host to be eaten by the correct type of predator. Such parasites should benefit from an ability to suppress the host’s fear of predators, but if the manipulation is imprecise the consequence may be increased predation by non-hosts, to the detriment of the parasite. Three-spined sticklebacks (Gasterosteus aculeatus) infected by the cestode Schistocephalus solidus express reduced antipredator behaviours, but it is unknown whether this is an example of a highly precise manipulation, a more general manipulation, or if it can even be attributed to mere side effects of disease. In a series of experiments, we investigated several behaviours of infected and uninfected sticklebacks. As expected, they had weak responses to simulated predatory attacks compared to uninfected fish. However, our results suggest that the parasite induced a general fearlessness, rather than a precise manipulation aimed at the correct predators (birds). Infected fish had reduced responses also when attacked from the side and when exposed to odour from a fish predator, which is a “dead-end” for this parasite. We also tested whether the reduced anti-predator behaviours were mere symptoms of a decreased overall vigour, or due to parasite-induced hunger, but we found no support for these ideas. We propose that even imprecise manipulations of anti-predator behaviours may benefit parasites, for example, if other behaviours are altered in a way that increases the exposure to the correct predator.

Helminth-host-environment interactions: Looking down from the tip of the iceberg

“…Although this promotes transmission to the definitive host, infected sticklebacks are also more susceptible to predation by non-host predators (Svensson et al . 2022).…”

“…Of note, it now seems that the increased susceptibility of S. solidusinfected three-spined stickleback to predation results from a generalized lethargy. Although this promotes transmission to the definitive host, infected sticklebacks are also more susceptible to predation by non-host predators (Svensson et al 2022).…”

Time-course of antipredator behavioral changes induced by the helminthPomphorhynchus laevisin its intermediate hostGammarus pulex: the switch in manipulation according to parasite developmental stage differs between behaviors

“…(Bethel & Holmes, 1977;Moore, 1983;Lagrue et al, 2007), reviewed, for example, in Poulin (2010. These parasites generally alter the antipredator behaviors of their intermediate hosts (Svensson et al, 2022), and some parasites are even able to reverse their intermediate host's fear of predator cues (Berdoy et al, 2000;Perrot-Minnot et al, 2007). These host behavioral changes favoring parasite transmission are seen as an extended phenotype of parasites and are often referred as parasitic manipulation (Hughes et al, 2012).…”

Time-course of antipredator behavioral changes induced by the helminth Pomphorhynchus laevis in its intermediate host Gammarus pulex: the switch in manipulation according to parasite developmental stage differs between behaviors

“…(Bethel & Holmes, 1977;Moore, 1983;Lagrue et al, 2007), reviewed, for example, in Poulin (2010). These parasites generally alter the antipredator behaviors of their intermediate hosts (Svensson et al, 2022), and some parasites are even able to reverse their intermediate host's fear of predator cues (Berdoy et al, 2000;Perrot-Minnot et al, 2007). These host behavioral changes favoring parasite transmission are adaptive for parasites but detrimental to the host.…”