A parasite's modification of host behavior reduces predation on its host

Abstract

Parasite modification of host behavior is common, and the literature is dominated by demonstrations of enhanced predation on parasitized prey resulting in transmission of parasites to their next host. We present a case in which predation on parasitized prey is reduced. Despite theoretical modeling suggesting that this phenomenon should be common, it has been reported in only a few host–parasite–predator systems. Using a system of gregarine endosymbionts in host mosquitoes, we designed experiments to compare the vulnerability of parasitized and unparasitized mosquito larvae to predation by obligate predatory mosquito larvae and then compared behavioral features known to change in the presence of predatory cues. We exposed Aedes triseriatus larvae to the parasite Ascogregarina barretti and the predator Toxohrynchites rutilus and assessed larval mortality rate under each treatment condition. Further, we assessed behavioral differences in larvae due to infection and predation stimuli by recording larvae and scoring behaviors and positions within microcosms. Infection with gregarines reduced cohort mortality in the presence of the predator, but the parasite did not affect mortality alone. Further, infection by parasites altered behavior such that infected hosts thrashed less frequently than uninfected hosts and were found more frequently on or in a refuge within the microcosm. By reducing predation on their host, gregarines may be acting as mutualists in the presence of predation on their hosts. These results illustrate a higher‐order interaction, in which a relationship between a species pair (host–endosymbiont or predator–prey) is altered by the presence of a third species.

Infection byParorchis acanthus(Trematoda) decreases grazing by the keystone gastropod,Littoraria irrorata

“…A broad body of research demonstrates the ability of parasites to induce powerful changes in the behavior of their hosts ( Holmes & Bethel, 1972 ; Dobson, 1988 ; Moore & Gotelli, 1990 ; Lafferty & Morris, 1996 ; Moore, 2002 ; Toscano, Newsome & Griffen, 2014 ; Soghigian, Valsdottir & Livdahl, 2017 ). These changes may be adaptive for the parasite because behavioral modification often facilities transmission to the next host species in its life cycle, an adaptive response of the host species, or a non-adaptive byproduct of parasitic infection ( Lafferty, 1999 ; Levri, 1999 ; Moore, 2002 ).…”

Differential response to mosquito host sex and parasite dosage suggest mixed dispersal strategies in the parasite Ascogregarina taiwanensis

“…Sexual reproduction occurs there through syzygy [ 24 ] and resulting oocysts remain in the host until eclosion; some parasites are released back into the larval environment upon emergence, while others are carried with adults and released during defecation or oviposition [ 29 ]. Virulence within natural hosts appears to be so low that some authors have suggested that these parasites are largely benign [ 27 , 29 , 33 ], and a recent study has shown that Ascogregarina may alter larval feeding behaviors and reduce risk of predation on their hosts [ 34 ]. However, environmental factors such as food availability and dosage of parasites can lead to elevated mortality rates and developmental delay in aquatic stages of the mosquito and reduced body size in adults [ 35 – 37 ].…”

Parasitism of Aedes albopictus by Ascogregarina taiwanensis lowers its competitive ability against Aedes triseriatus.

“…barretti were killed less often by a predator, Toxohrynchites rutilus, than compared to uninfected Ae. triseriatus [56]. This shows that while the effect of the parasite does have an effect on the competition between the two species, there are other species which might exacerbate or mitigate the effects of As.…”