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. 2022 Jan 19:11:e71503.
doi: 10.7554/eLife.71503.

Both consumptive and non-consumptive effects of predators impact mosquito populations and have implications for disease transmission

Marie C Russell #  1 , Catherine M Herzog #  2 , Zachary Gajewski  3 , Chloe Ramsay  4 , Fadoua El Moustaid  3 , Michelle V Evans  5   6 , Trishna Desai  7 , Nicole L Gottdenker  5   8 , Sara L Hermann  9 , Alison G Power  10 , Andrew C McCall  11
Affiliations

Both consumptive and non-consumptive effects of predators impact mosquito populations and have implications for disease transmission

Marie C Russell et al. Elife. .

Abstract

Predator-prey interactions influence prey traits through both consumptive and non-consumptive effects, and variation in these traits can shape vector-borne disease dynamics. Meta-analysis methods were employed to generate predation effect sizes by different categories of predators and mosquito prey. This analysis showed that multiple families of aquatic predators are effective in consumptively reducing mosquito survival, and that the survival of Aedes, Anopheles, and Culex mosquitoes is negatively impacted by consumptive effects of predators. Mosquito larval size was found to play a more important role in explaining the heterogeneity of consumptive effects from predators than mosquito genus. Mosquito survival and body size were reduced by non-consumptive effects of predators, but development time was not significantly impacted. In addition, Culex vectors demonstrated predator avoidance behavior during oviposition. The results of this meta-analysis suggest that predators limit disease transmission by reducing both vector survival and vector size, and that associations between drought and human West Nile virus cases could be driven by the vector behavior of predator avoidance during oviposition. These findings are likely to be useful to infectious disease modelers who rely on vector traits as predictors of transmission.

Keywords: disease dynamics; ecology; epidemiology; global health; meta-analysis; mosquito; predation; vector ecology.

Plain language summary

Mosquitoes are often referred to as the deadliest animals on earth because some species spread malaria, West Nile virus or other dangerous diseases when they bite humans and other animals. Adult mosquitoes fly to streams, ponds and other freshwater environments to lay their eggs. When the eggs hatch, the young mosquitoes live in the water until they are ready to grow wings and transform into adults. In the water, the young mosquitoes are particularly vulnerable to being eaten by dragonfly larvae, fish and other predators. When adult females are choosing where to lay their eggs, they can use their sense of smell to detect these predators and attempt to avoid them. Along with eating the mosquitoes, the predators may also reduce mosquito populations in other ways. For example, predators can disrupt feeding among young mosquitoes, which may affect the time that it takes for them to grow into adults or the size of their bodies once they reach the adult stage. Although the impacts of different predators have been tested separately in multiple settings, the overall effects of predators on the ability of mosquitoes to spread diseases to humans remain unclear. To address this question, Russell, Herzog et al. used an approach called meta-analysis on data from previous studies. The analysis found that along with increasing the death rates of mosquitoes, the presence of predators also leads to a reduction in the body size of those mosquitoes that survive, causing them to have shorter lifespans and fewer offspring. Russell, Herzog et al. found that one type of mosquito known as Culex – which carries West Nile virus – avoided laying its eggs near predators. During droughts, increased predation in streams, ponds and other aquatic environments may lead adult female Culex mosquitoes to lay their eggs closer to residential areas with fewer predators. Russell, Herzog et al. propose that this may be one reason why outbreaks of West Nile virus in humans are more likely to occur during droughts. In the future, these findings may help researchers to predict outbreaks of West Nile virus, malaria and other diseases carried by mosquitoes more accurately. Furthermore, the work of Russell, Herzog et al. provides examples of mosquito predators that could be used as biocontrol agents to decrease numbers of mosquitoes in certain regions.

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Conflict of interest statement

MR, CH, ZG, CR, FE, ME, TD, NG, SH, AP, AM No competing interests declared

Figures

Figure 1.
Figure 1.. Flowchart demonstrating the literature search, screening process, data exclusions, and the resulting seven different vector trait data subsets.
Figure 2.
Figure 2.. Mosquito predator classes (bold font) and families (italicized font) included in the database and the vector traits that they may influence (in parentheses); predator images not to scale, and placed randomly with respect to the different mosquito life stages.
Image sources: phylopic.org (CC BY 3.0 or public domain): Actinopterygii (creator: Milton Tan), Arachnida (creators: Sidney Frederic Harmer & Arthur Everett Shipley, vectorized by Maxime Dahirel), Branchiopoda (creator: Africa Gomez), and Insecta (creator: Marie Russell). BioRender.com: Amphibia, Hexanauplia, and Malacostraca class silhouettes; mosquito larval instars, pupa, and blood-feeding adult. Trishna Desai: mosquito egg raft.
Figure 3.
Figure 3.. Effect sizes and 95 % confidence intervals for consumptive effects of predators, for different categories of moderators (with number of studies in parentheses).
(a) predator family with predator class in the right-hand column, (b) vector genus, and (c) larval instar.
Figure 4.
Figure 4.. Oviposition effect sizes and 95 % confidence intervals for different categories of vector genus (with number of studies in parentheses).
See this image and copyright information in PMC

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