Host reproductive phenology drives seasonal patterns of host use in mosquitoes

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).

Figure 1. Host reproduction and mosquito parasitism.

Seasonal patterns of relative host use (left y axis) and reproductive investment (mean ± SE) in white-tailed deer (a), great blue heron (b), and yellow-crowned night heron (c). Relative host use, the proportion of blood meals (± SE) originating from a given host in a semimonthly period, was determined by PCR-based assays identifying the vertebrate source of blood from field-collected mosquitoes over seven years (2001–2004 and 2006–2008). The number of bloodmeals identified in a period is given on the x axis.

Figure 2. Mate attraction and mosquito parasitism of frogs.

Phenology of detectability (vocalizing males) and relative anuran host use by mosquitoes (right y axis). Relative host use, the proportion of blood meals (± SE) originating from (a) early-breeding (Spring Peeper, Leopard frog) and (b) late-breeding (Bullfrog, Green frog, Green treefrog, Grey treefrog, Pine woods treefrog) frogs, was determined by PCR-based assays identifying the vertebrate source of blood from field-collected mosquitoes over seven years (2001–2004 and 2006–2008) from a study site in Alabama, USA. Mean detectability (± SE) was calculated from monthly detection probabilities of each breeding cohort, using general linear mixed models with a binomial distribution and a logit-link. The number of bloodmeals identified in each month is given on the x axis.