Diel periodicity and visual cues guide oviposition behavior in Phlebotomus papatasi, vector of old-world cutaneous leishmaniasis

• Published in: PLoS neglected tropical diseases Vol. 13; no. 3; p. e0007165
• Main Authors: Shymanovich, Tatsiana, Faw, Lindsey, Hajhashemi, Nima, Teague, Jimmie, Schal, Coby, Ponnusamy, Loganathan, Apperson, Charles S, Hatano, Eduardo, Wasserberg, Gideon
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 01.03.2019; Public Library of Science (PLoS)
• Subjects: Animals; Attraction; Behavioural responses; Biology; Biology and Life Sciences; Chemoreception; Circadian Clocks; Color; Colour; Containers; Crepuscular; Cues; Cutaneous leishmaniasis; Darkness; Diel periodicity; Diptera; Disease transmission; Distribution; Engineering and Technology; Entomology; Environmental aspects; Female; Females; Flies; Flight tests; Free flight; Generalized linear models; Health aspects; Humans; Illumination; Insect Control; Insect Vectors - anatomy & histology; Insect Vectors - physiology; Insecticides; Insects; Leishmaniasis; Leishmaniasis - transmission; Light; Malaria; Medical research; Medicine and Health Sciences; Mosquitoes; Night; Olfaction; Olfactory stimuli; Ova; Oviposition; Parasitic diseases; Periodicity; Phlebotomus - anatomy & histology; Phlebotomus - physiology; Phlebotomus papatasi; Photoperiod; Photoperiods; Physical Sciences; Plant pathology; Reproductive strategy; Screens; Sex Attractants; Sexual behavior; Site selection; Social Sciences; Test chambers; Time of use; Tropical climate; Tropical diseases; Vector-borne diseases; Vectors; Visual effects; Visual stimuli; Women; United States; North Carolina; United States > US; Israel
• ISSN: 1935-2735; 1935-2727; 1935-2735
• DOI: 10.1371/journal.pntd.0007165

Phlebotomine sand flies are vectors of human leishmaniases, important neglected tropical diseases. In this study, we investigated diel patterns of oviposition behavior, effects of visual cues on oviposition-site selection, and whether these affect the attraction of gravid Phlebotomus papatasi (Scopoli), the vector of old-world cutaneous leishmaniasis, to olfactory cues from oviposition sites. To evaluate these questions, we conducted a series of experiments using attraction and oviposition assays within free-flight test chambers containing gravid females entrained under a 14:10 hrs light:dark photoperiod. By replacing sticky-screens or moist filter papers every three hours, we showed that oviposition site search occurs mainly in the latest part of the night whereas peak oviposition occurs during the early part of the night. Behavioral responses to olfactory oviposition cues are regulated by time-of-day and can be disrupted by transient exposure to a constant darkness photoperiod. Gravid females, but not any other stage, age, or sex, were attracted to dark, round oviposition jars, possibly resembling rodent burrow openings. This visual attraction disappeared in the absence of an illumination source. Egg deposition rate was not affected by jar color. Olfactory cues had the strongest effect when the visual cues were minimal. Our study showed, for the first time, that visual cues in the form of oviposition-site color, lighting level, and photoperiod are important in guiding the oviposition behavior of phlebotomine sand flies. Furthermore, such visual cues could modify the flies' sensitivity to olfactory oviposition cues. Our results suggest that chemosensory and visual cues are complementary, with visual cues used to orient gravid females towards oviposition sites, possibly at long- to medium-ranges during crepuscular periods, while olfactory cues are used to approach the burrow in darkness and assess its suitability at close-range. Implications to sand fly control are discussed.