Mosquito Oviposition Behavior and Vector Control

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Mosquito Oviposition Behavior and Vector Control insects Review Mosquito Oviposition Behavior and Vector Control Jonathan F. Day Florida Medical Entomology Laboratory, University of Florida, IFAS, 200 9th St. SE, Vero Beach, FL 32962, USA; jfda@ufl.edu; Tel.: +1-772-778-7200 (ext. 132) Academic Editor: Walter J. Tabachnick Received: 1 September 2016; Accepted: 31 October 2016; Published: 18 November 2016 Abstract: The burden of gene transfer from one mosquito generation to the next falls on the female and her eggs. The selection of an oviposition site that guarantees egg and larval survival is a critical step in the reproductive process. The dangers associated with ephemeral aquatic habitats, lengthy droughts, freezing winters, and the absence of larval nutrition makes careful oviposition site selection by a female mosquito extremely important. Mosquito species exhibit a remarkable diversity of oviposition behaviors that ensure eggs are deposited into microenvironments conducive for successful larval development and the emergence of the next mosquito generation. An understanding of mosquito oviposition behavior is necessary for the development of surveillance and control opportunities directed against specific disease vectors. For example, Aedes aegypti Linnaeus is the vector of viruses causing important human diseases including yellow fever, dengue, chikungunya, and Zika. The preference of this species to oviposit in natural and artificial containers has facilitated the development of Ae. aegypti-specific surveillance and toxic oviposition traps designed to detect and control this important vector species in and around disease foci. A better understanding of the wide diversity of mosquito oviposition behavior will allow the development of new and innovative surveillance and control devices directed against other important mosquito vectors of human and animal disease. Keywords: mosquito oviposition; mosquito control; mosquito-borne disease transmission 1. Introduction Anautogenous female mosquitoes must blood feed to acquire the protein necessary to develop a batch of eggs. Blood meal digestion is temperature-dependent and takes 2 to 3 days in the tropics and 5 to 8 days in temperate environments [1] (pp. 222–285). Products from blood meal digestion (such as amino acids) are absorbed by the fat body, which in turn synthesizes and releases vitellogenin (Vg), a glycophospolipoprotein, into the hemolymph. The Vg is transported to the ovaries and where it is absorbed by oocytes in the follicular epithelia. Female mosquitoes are considered to be gravid, sometimes containing as many as 250 eggs, when the oocytes are replete. Gravid females initiate oviposition searching flights that correspond with their normal daily activity periods. Many mosquito species oviposit during the dawn and dusk crepuscular periods. Even though mosquitoes have fixed circadian activity periods, environmental factors ultimately control their flight patterns. Meteorological conditions including temperature, rainfall, relative humidity, and wind determine when gravid females fly and where they oviposit. In general, warm, moist, humid, and calm conditions favor mosquito flight and oviposition [2]. Once in flight, gravid females rely on visual [2,3] and olfactory cues to identify potential oviposition sites. As a site is approached, visual, olfactory, and finally tactile cues are used to evaluate the quality of the site for oviposition. The chemical ecology of mosquito oviposition was reviewed by Bentley and Day [4] and is a source of additional information concerning many aspects of mosquito oviposition behavior. It can take a gravid female days, weeks, or even months to locate a suitable oviposition site. Delayed oviposition may affect disease transmission by mosquitoes Insects 2016, 7, 65; doi:10.3390/insects7040065 www.mdpi.com/journal/insects Insects 2016, 7, 65 2 of 22 infected with nematode, protozoan, or viral pathogens. Once ingested, the pathogen undergoes an extrinsic incubation period (EIP) that involves migration out of the blood meal, penetration of the midgut, replication within mosquito cells, and invasion of the mosquito’s body tissues including the salivary glands, a process that may take from 7 to 30 days and is usually temperature-dependent. Because blood digestion is a short process, usually less than a week, it is unlikely that the EIP will be completed before digestion of the blood meal in which the pathogen was acquired. When oviposition is delayed, the EIP may be completed before the first egg batch is laid, thus allowing disease transmission after a single gonotrophic cycle [5]. An understanding of the biological factors associated with mosquito oviposition provides opportunities for the design of highly effective, species-specific mosquito surveillance and control protocols. For example, the preference of some Culex species to lay eggs in highly organic freshwater pools has been exploited to develop efficient traps (gravid traps) [6] to monitor mosquito populations responsible for the transmission of St. Louis encephalitis and West Nile viruses. Likewise, the preference of Aedes aegypti to oviposit in artificial containers was used to develop ovitraps for the surveillance and control of local populations of this mosquito species in Australia [7]. The diversity of mosquito oviposition behavior provides some of the most interesting examples of adaptation in the natural world. Strategies and adaptations including skip oviposition, where females scatter an egg batch between different oviposition sites; morphological adaptation, where a narrowing of the thorax allows females access to oviposition sites through extremely small holes; and egg-brooding, where females guard and protect their eggs, are all factors that ensure mosquito larval development in favorable habitats. The natural history of mosquito oviposition including oviposition site location and evaluation, physiological factors that affect oviposition, circadian oviposition behavior, mosquito egg-hatching strategies, and how an understanding of mosquito oviposition can be used to develop novel mosquito surveillance and control techniques are the subjects of this review. 2. The Natural History of Mosquito Oviposition 2.1. Oviposition Site Location There are presently 3550 mosquito species recognized worldwide that are contained in two subfamilies, 11 tribes, and 112 genera [8]. Mosquitoes deposit two basic types of eggs: Rapid-Hatch (RH) and Delayed-Hatch (DH). Rapid-Hatch eggs are deposited directly into water, on the water surface, or on substrate close to the water and usually hatch within 48 h. The RH eggs are laid individually, in small groups, or in rafts containing up to several hundred eggs. Delayed Hatch eggs are usually deposited singly or in small groups, are drought-resistant, survive for long periods out of the water, hatch soon after being re-flooded, and sometimes enter a photoperiod-induced diapause to survive temperate and arctic winters. Examples of mosquito egg laying behavior and the types of eggs deposited are presented in Table1. Based on mosquito flight behavior in Florida, USA, Bidlingmayer [9] grouped species into three broad categories according to flight preference: (1) Field mosquitoes occurred most frequently in habitats such as new fields, open salt marshes, and pine flatwoods; all habitats with little understory vegetation. These species occurred in lowest numbers in densely vegetated habitats. Field mosquitoes avoided trees and shrubs and were taken in large numbers in light traps set in open habitats. Examples of field species include Aedes taeniorhynchus (Wiedemann), Ae. vexans (Miegen), Anopheles crucians Wiedemann, and Uranotaenia sapphirina (Osten Sacken); (2) Woodland mosquitoes preferred forested habitats, avoided open areas during dry periods, and were less likely to enter light traps. Examples of woodland mosquitoes include Culiseta melanura (Coquillett) and Psorophora ferox (Von Humboldt); (3) Edge mosquitoes preferred ecotone habitats and were intermediate in their response to light traps. Edge mosquitoes include An. quadrimaculatus Say and Coquillettidia perturbans (Walker). Bidlingmayer and Hem [10] later added a forth group, commuter mosquitoes. These species rested in woodland habitats during the day, but foraged in open habitats during the evening crepuscular, nocturnal, Insects 2016, 7, 65 3 of 22 and morning crepuscular periods. Culex nigripalpus Theobald is an example of a commuter species. Gillies [11] in an earlier publication classified mosquitoes into four groups based on their flight behavior. His first two groups were equivalent to Bidlingmayer’s field and woodland mosquitoes but Gillies included two additional groups; domestic mosquitoes, such as Ae. aegypti, and cave mosquitoes including Cx. pipiens molestus Forskal. Table 1. Mosquito oviposition: examples of egg laying behavior [1,8]. Method of Oviposition Tribe Genera Species Anopheles Meigen Anopheles atroparvus Van Thiel Anopheles gambiae Giles Sabethes Sabethini Sabethes chloropterus (Von Humboldt) In flight emission of Robineau-Desvoidy single eggs to the oviposition site Sabethini Tripteroides Giles Tripteroides aranoides (Theobald) Sabethini Topomyia Leicester Topomyia yanbarensis Miyagi Sabethini Wyeomyia Theobald Wyeomyia vanduzeei Dyar and Knab Toxorhynchitini Toxorhynchites Theobald Toxorhynchites amboinensis (Doleschall) Aedini Aedes Meigen Aedes aegypti (Linnaeus) Aedini Aedes Meigen Aedes triseriatus (Say) Desiccation-resistant Aedini Armigeres Theobald Armigeres subalbatus (Coquillett) eggs laid singly on moist Culicini Deinocerites
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