Aquatic microfauna alter larval food resources and affect development and biomass of West Nile and Saint Louis encephalitis vector Culex nigripalpus (Diptera: Culicidae).

Dagne Duguma,Arthur B. Simas Domingos,Michael G. Kaufman

doi:10.1002/ece3.2947

Dagne Duguma, Arthur B. Simas Domingos + Show 1 more

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https://doi.org/10.1002/ece3.2947

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Abstract

Ciliate protists and rotifers are ubiquitous in aquatic habitats and can comprise a significant portion of the microbial food resources available to larval mosquitoes, often showing substantial declines in abundance in the presence of mosquito larvae. This top‐down regulation of protists is reported to be strong for mosquitoes inhabiting small aquatic containers such as pitcher plants or tree holes, but the nature of these interactions with larval mosquitoes developing in other aquatic habitats is poorly understood. We examined the effects of these two microbial groups on lower trophic level microbial food resources, such as bacteria, small flagellates, and organic particles, in the water column, and on Culex larval development and adult production. In three independent laboratory experiments using two microeukaryote species (one ciliate protist and one rotifer) acquired from field larval mosquito habitats and cultured in the laboratory, we determined the effects of Culex nigripalpus larval grazing on water column microbial dynamics, while simultaneously monitoring larval growth and development. The results revealed previously unknown interactions that were different from the top‐down regulation of microbial groups by mosquito larvae in other systems. Both ciliates and rotifers, singly or in combination, altered other microbial populations and inhibited mosquito growth. It is likely that these microeukaryotes, instead of serving as food resources, competed with early instar mosquito larvae for microbes such as small flagellates and bacteria in a density‐dependent manner. These findings help our understanding of the basic larval biology of Culex mosquitoes, variation in mosquito production among various larval habitats, and may have implications for existing vector control strategies and for developing novel microbial‐based control methods.

Highlights

The interactions of these microeukaryotes with mosquito larvae mainly as a top predator have been well studied in phytotelmata such as in pitcher plants Sarracenia purpurea L. and in tree hole systems (Addicott, 1974; Cochran-Stafira & von Ende, 1998; Eisenberg, Washburn, & Schreiber, 2000; Hoekman, 2007, 2011; Walker, Kaufman, & Merritt, 2010; Washburn, 1995). This knowledge is largely limited to species of Aedes or Wyeomyia mosquitoes inhabiting small container mosquito habitats, and less is known about the interaction of these microbes with other mosquito taxa. Both protists and rotifers primarily feed on bacteria (Gatesoupe, 1991; Pernthaler, 2005; Wallace & Smith, 2013), whereas mosquito larvae are considered omnivores feeding on varied microorganisms including protists and rotifers, as well as bacteria, fungi, and microalgae (Merritt, Dadd, & Walker, 1992)
A previous study that removed Culex mosquito larvae from the water column using a larvicide detected trophic cascade effects in the water column, but that study did not address whether population dynamics of heterotrophic microeukaryotes were altered as a result of reduced larval mosquito abundance (Duguma et al, 2015)
This suggests that mortality of conspecific larvae did not release remaining larvae from competition and that the survivors continued to compete with the added microeukaryotes for resources, while further investigation is required to determine the exact causes of the reduced adult size in this study in microeukaryote treatments compared to the untreated controls, it points out another possible factor in larval habitats that can influence production and disease transmission capacity of mosquito vectors

Summary

| INTRODUCTION

Heterotrophic microorganisms such as protists and rotifers are ubiquitous in aquatic mosquito larval habitats and are important components of the microbial food web that is a primary nutritional resource for larvae, in container-type larval mosquito habitats The interactions of these microeukaryotes with mosquito larvae mainly as a top predator have been well studied in phytotelmata such as in pitcher plants Sarracenia purpurea L. and in tree hole systems (Addicott, 1974; Cochran-Stafira & von Ende, 1998; Eisenberg, Washburn, & Schreiber, 2000; Hoekman, 2007, 2011; Walker, Kaufman, & Merritt, 2010; Washburn, 1995) This knowledge is largely limited to species of Aedes or Wyeomyia mosquitoes inhabiting small container mosquito habitats, and less is known about the interaction of these microbes with other mosquito taxa. We characterized the abundance of lower trophic level microorganisms such as bacteria and sized microbes in the presence or absence of a ciliate and rotifer species isolated from larval Cx. nigripalpus habitats

| MATERIAL AND METHODS

| DISCUSSION

Findings

| CONCLUSIONS