The effects of oviposition-site deprivation on Anopheles gambiae reproduction

Abstract

BackgroundThe African malaria mosquito, Anopheles gambiae, depends on availability of suitable surface water for oviposition. Short and long dry spells occur throughout the year in many parts of its range that limit its access to oviposition sites. Although not well understood, oviposition-site deprivation has been found to rapidly reduce egg batch size and hatch rate of several mosquito species. We conducted laboratory experiments to assess these effects of oviposition-site deprivation on An. gambiae and to evaluate the role of nutrition and sperm viability as mediators of these effects.MethodsAnopheles gambiae adults (1–2 d old) from the G3 laboratory colony were assigned to the following treatment groups: oviposition-deprived (fed once and then deprived of oviposition site for 7 or 14 d), multiple-fed control (fed regularly once a week and allowed to lay eggs without delay), and age matched blood-deprived control (fed once, three days before water for oviposition was provided). Egg batch size and hatch rate were measured. In the second experiment two additional treatment groups were included: oviposition-deprived females that received either a second (supplemental) blood meal or virgin males (supplemental mating) 4 days prior to receiving water for oviposition.ResultsAn. gambiae was highly sensitive to oviposition-site deprivation. Egg batch size dropped sharply to 0–3.5 egg/female within 14 days, due to reduced oviposition rate rather than a reduced number of eggs/batch. Egg hatch rate also fell dramatically to 0-2% within 7 days. The frequency of brown eggs that fail to tan was elevated. A supplemental blood meal, but not ‘supplemental insemination,’ recovered the oviposition rate of females subjected to oviposition-site deprivation. Similarly, a supplemental blood meal, but not ‘supplemental insemination,’ partly recovered hatch rate, but this increase was marginally significant (P < 0.069).ConclusionsEven a short dry spell resulting in oviposition-site deprivation for several days may result in a dramatic decline of An. gambiae populations via reduced fecundity and fertility. However, females taking supplemental blood meals regain at least some reproductive success. If mosquitoes subjected to oviposition-site deprivation increase the frequency of blood feeding, malaria transmission may even increase during a short dry spell. The relevance of oviposition-site deprivation as a cue to alter the physiology of An. gambiae during the long dry season is not evident from these results because no reduction in hatch rate was evident in wild M-form An. gambiae collected in the dry season in the Sahel by previous studies.

Ecophysiology of Anopheles gambiae s.l.: Persistence in the Sahel

“…Consistent with aestivation rather than with quiescence, the switch from reproduction to long-term survival was not a direct result of the absence of surface water for oviposition (Artis et al, 2014; Dieter et al, 2012), indicating that a token environmental stimulus is involved. Accordingly, An.…”

“…As noted above, studies using the G3 colony of An. gambiae showed that oviposition-site deprivation alone was insufficient to shift mosquitoes into reproductive quiescence and extended longevity (Artis et al, 2014; Dieter et al, 2012). During the dry season, Anopheles funestus exhibited a reduced proportion of gravid females and a higher proportion of partly blood-fed females compared with wet season, suggesting that reproduction is suppressed in at least a fraction of the population (Charlwood et al, 2013).…”

The contribution of dietary restriction to extended longevity in the malaria vector Anopheles coluzzii

“…Blood and sugar access were arbitrarily provided per treatment on different schedules as described below (Table 2). Based on our insectary blood-feeding schedule of once per 7 days, this interval was selected as the standard for non-restricted blood diet [73, 74]. Blood meals took place between 5–6 pm in a darkened room at 27 °C, 80% RH.…”

“…Dry-season treatments (50% RH) were not provided with oviposition water, i.e. were subjected to oviposition site deprivation [74]. Handling and maintenance of the cages was minimized as much as possible to reduce human interference and subsequent stress in the mosquitoes.…”

Plasmodiuminfection brings forward mosquito oviposition

“…Here, we test whether Plasmodium-infected mosquitoes oviposit earlier than their non-infected counterparts. To do so, we use the Culex pipiens-Plasmodium relictum system, which combines a mosquito characterized by its strong flexibility regarding the timing of egg-laying [9,10] and a parasite that drastically reduces its fecundity [3]. Bringing forward the age of oviposition is expected to come at a cost, which only the fittest mosquitoes may be able to bear.…”