Avian malaria infection intensity influences mosquito feeding patterns

Abstract

Pathogen-induced host phenotypic changes are widespread phenomena that can dramatically influence host-vector interactions. Enhanced vector attraction to infected hosts has been reported in a variety of host-pathogen systems, and has given rise to the parasite manipulation hypothesis whereby pathogens may adaptively modify host phenotypes to increase transmission from host to host. However, host phenotypic changes do not always favour the transmission of pathogens, as random host choice, reduced host attractiveness and even host avoidance after infection have also been reported. Thus, the effects of hosts' parasitic infections on vector feeding behaviour and on the likelihood of parasite transmission remain unclear. Here, we experimentally tested how host infection status and infection intensity with avian Plasmodium affect mosquito feeding patterns in house sparrows (Passer domesticus). In separate experiments, mosquitoes were allowed to bite pairs containing (i) one infected and one uninfected bird and (ii) two infected birds, one of which treated with the antimalarial drug, primaquine. We found that mosquitoes fed randomly when exposed to both infected and uninfected birds. However, when mosquitoes were exposed only to infected individuals, they preferred to bite the non-treated birds. These results suggest that the malarial parasite load rather than the infection itself plays a key role in mosquito attraction. Our findings partially support the parasite manipulation hypothesis, which probably operates via a reduction in defensive behaviour, and highlights the importance of considering parasite load in studies on host-vector-pathogen interactions.

Patterns of avian haemosporidian infections vary with time, but not habitat, in a fragmented Neotropical landscape

“…Rather, the low prevalence observed could be the result of a drastic fragmentation in the region or the fact that most of our sampling was conducted during the dry season. Because parasite load is closely associated with the feeding behavior of mosquito vectors [ 81 , 82 ] the inclusion of parasite load instead of parasite prevalence as the proxy for parasite infection may shed new light on understanding the relationship between habitat loss and parasite infection in the area. Finally, the finding of an association between seasonality and avian malaria infections highlights the importance of this factor in future studies, particularly when working in the tropics.…”

Is Host Selection by Mosquitoes Driving Vector Specificity of Parasites? A Review on the Avian Malaria Model

“…According to the vector adaptive avoidance (Lalubin et al, 2012), mosquitoes should avoid highly infected individuals due to the costs induced by parasite in the vectors. However, Yan et al (2018) found the opposite with mosquitoes feeding with a higher rate on those individuals that had a higher Plasmodium parasite load, suggesting a pre-eminence of parasite manipulation over vector avoidance. Comprehensive studies controlling for multiple factors are needed to better understand the interplay between these two opposite factors in the host selection by vectors.…”

“…pipiens system have obtained contradictory results. While some studies found that mosquitoes were attracted to, or fed on chronically infected birds at a higher rate than uninfected hosts (Cornet et al, 2013;Díez-Fernández et al, 2020), other studies have reported the opposite pattern (Lalubin et al, 2012) or an absence of significant differences between infected and uninfected birds (Yan et al, 2018;Gutiérrez-López et al, 2019). This discrepancy may come from the different experimental procedures used (e.g., either dual-choice olfactometer or direct contact with immobilized hosts) and therefore further studies are required to clarify how the infection status may influence the feeding behavior of mosquitoes.…”

“…As an example, Burkett-Cadena et al 2014found that mosquitoes had a higher feeding preference for male birds, but this result was observed mainly in mammophilic mosquitoes. On the other hand, several studies failed to find any significant sex-biased feeding pattern in ornithophilic mosquitoes (Simpson et al, 2009;Yan et al, 2018;Cozzarolo et al, 2019;Díez-Fernández et al, 2019;Gutiérrez-López et al, 2019). It has also been suggested that the composition of volatile substances from the uropygial gland secretions, which differ between male and female birds (Jacob et al, 1979;Amo et al, 2012), could affect the attraction of blood-sucking insects (Russell and Hunter, 2005; Martínez-de la Puente et al, 2011).…”

Effects of Chemical and Auditory Cues of Hoopoes (Upupa epops) in Repellence and Attraction of Blood-Feeding Flies

“…Different odors emitted by birds have been evaluated as attractants of vectors, from feces that attract mosquitoes (Cooperband et al, 2008) and biting midges (Fernandes-Rios et al, 2020), to bird feathers and skin that attract mosquitoes (Allan et al, 2006) and blackflies (Lowther and Wood, 1964;Weinandt et al, 2012). It has been also shown that mosquitoes are attracted to birds (Cornet et al, 2013a,b;Yan et al, 2018), or to odor from birds (Díez-Fernández et al, 2020), infected by avian malaria over non-infected or less infected birds (but see Tomás et al, 2008b;Martínez-de la Puente et al, 2009b;Lalubin et al, 2012 for contrasting results). However, chemical cues from the uropygial secretion apparently are not responsible for this mosquito response (Díez-Fernández et al, 2020).…”