Host Reproductive Phenology Drives Seasonal Patterns of Host Use in Mosquitoes

Nathan D Burkett-Cadena,Sean P Graham,Micky D Eubanks,Christopher J W Mcclure,Geoffrey E Hill,Stephen S Ditchkoff,Craig Guyer,Russell A Ligon,Thomas R Unnasch,Hassan K Hassan

doi:10.1371/journal.pone.0017681

Nathan D Burkett-Cadena, Sean P Graham + Show 8 more

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https://doi.org/10.1371/journal.pone.0017681

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Abstract

Seasonal shifts in host use by mosquitoes from birds to mammals drive the timing and intensity of annual epidemics of mosquito-borne viruses, such as West Nile virus, in North America. The biological mechanism underlying these shifts has been a matter of debate, with hypotheses falling into two camps: (1) the shift is driven by changes in host abundance, or (2) the shift is driven by seasonal changes in the foraging behavior of mosquitoes. Here we explored the idea that seasonal changes in host use by mosquitoes are driven by temporal patterns of host reproduction. We investigated the relationship between seasonal patterns of host use by mosquitoes and host reproductive phenology by examining a seven-year dataset of blood meal identifications from a site in Tuskegee National Forest, Alabama USA and data on reproduction from the most commonly utilized endothermic (white-tailed deer, great blue heron, yellow-crowned night heron) and ectothermic (frogs) hosts. Our analysis revealed that feeding on each host peaked during periods of reproductive activity. Specifically, mosquitoes utilized herons in the spring and early summer, during periods of peak nest occupancy, whereas deer were fed upon most during the late summer and fall, the period corresponding to the peak in births for deer. For frogs, however, feeding on early- and late-season breeders paralleled peaks in male vocalization. We demonstrate for the first time that seasonal patterns of host use by mosquitoes track the reproductive phenology of the hosts. Peaks in relative mosquito feeding on each host during reproductive phases are likely the result of increased tolerance and decreased vigilance to attacking mosquitoes by nestlings and brooding adults (avian hosts), quiescent young (avian and mammalian hosts), and mate-seeking males (frogs).

Highlights

Seasonal patterns of host selection by arthropods are a critical component in the amplification and spillover of arthropod-borne zoonoses [1]
Transmission of mosquito-borne viruses to humans usually occurs in late summer and early fall, when the mosquito population exhibits a shift in host use from birds to mammals [1,3]
A fourth hypothesis, that host-feeding patterns are due to seasonal changes in habitat use by mosquitoes, was indirectly supported by field evidence [5], but the authors neglected to demonstrate that mammals were more abundant in open habitats during times of mosquito foraging

Summary

Introduction

Seasonal patterns of host selection by arthropods are a critical component in the amplification and spillover of arthropod-borne zoonoses [1]. Mosquito-borne viruses, for example, circulate in populations of vertebrate reservoir hosts in annual periods of preepidemic virus amplification [2]. The hypothesis that hostfeeding patterns are due to seasonal changes in the abundance of avian hosts was not supported by field data from Florida [3]. A fourth hypothesis, that host-feeding patterns are due to seasonal changes in habitat use by mosquitoes (mosquitoes forage more often in open habitats when humidity is high and are more likely to encounter hosts in open habitats), was indirectly supported by field evidence [5], but the authors neglected to demonstrate that mammals were more abundant in open habitats during times of mosquito foraging. Apart from host abundance, none of the above studies examined the role of host biology in driving seasonal patterns of host use by mosquitoes, despite evidence that host biology affects defensive behaviors [7], a major factor in determining mosquito feeding success [8,9]

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