The effects of oviposition-site deprivation on Anopheles gambiae reproduction

Kathryne L. Dieter1, Diana L. Huestis1, Tovi Lehmann1
1Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, 12735 Twinbrook Parkway, Room 2W-09-C, Rockville, MD, 20852, USA

Tóm tắt

Abstract Background The 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. Methods Anopheles 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. Results An. 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). Conclusions Even 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.

Từ khóa


Tài liệu tham khảo

Simard F, Lehmann T, Lemasson JJ, Diatta M, Fontenille D: Persistence of Anopheles arabiensis during the severe dry season conditions in Senegal: an indirect approach using microsatellite loci. Insect Mol Biol. 2000, 9: 467-479. 10.1046/j.1365-2583.2000.00210.x.

Beier JC, Copeland RS, Oyaro C, Masinya A, Odago WO, Odour S, Koech DK, Roberts CR: Anopheles gambiae complex egg stage survival in dry soil from larval development sites in western Kenya. J Am Mosq Control Assoc. 1990, 6: 105-109.

Charlwood JD, Vij R, Billingsley PF: Dry season refugia of malaria-transmitting mosquitoes in a dry savannah zone of east Africa. AmJTrop Med Hyg. 2000, 62: 726-732.

Minakawa N, Githure JI, Beier JC, Yan G: Anopheline mosquito survival strategies during the dry period in western Kenya. J Med Entomol. 2001, 38: 388-392. 10.1603/0022-2585-38.3.388.

Sogoba N, Doumbia S, Vounatsou P, Baber I, Keita M, Maiga M, Traore SF, Toure A, Dolo G, Smith T, Ribeiro JM: Monitoring of larval habitats and mosquito densities in the Sudan savanna of Mali: implications for malaria vector control. AmJTrop Med Hyg. 2007, 77: 82-88.

Toure YT, Petrarca V, Traore SF, Coulibaly A, Maiga HM, Sankare O, Sow M, Di Deco MA, Coluzzi M: Ecological genetic studies in the chromosomal form Mopti of Anopheles gambiae s.s. in Mali, West Africa. Genetica. 1994, 94: 213-223. 10.1007/BF01443435.

Yang P: Effect of oviposition site deprivation on oviposition performance and egg hatch rate of naturally blood–fed gravid Culex quinquefasciatus (Diptera: Culicidae). Proceeding of the Hawaiian Entomol Society. 2008, 40: 51-54.

Adamou A, Dao A, Timbine S, Kassogue Y, Yaro AS, Diallo M, Traore SF, Huestis DL, Lehmann T: The contribution of aestivating mosquitoes to the persistence of Anopheles gambiae in the Sahel. Malaria J. 2011, 10: 151-10.1186/1475-2875-10-151.

Huestis DL, Yaro AS, Traore AI, Adamou A, Kassogue Y, Diallo M, Timbine S, Dao A, Lehmann T: Variation in metabolic rate of Anopheles gambiae and A. arabiensis in a Sahelian village. J Exp Biol. 2011, 214: 2345-2353. 10.1242/jeb.054668.

Huestis DL, Yaro AS, Traore AI, Dieter KL, Nwagbara JI, Bowie AC, Adamou A, Kassogue Y, Diallo M, Timbine S: Seasonal variation in metabolic rate, flight activity and body size of Anopheles gambiae in the Sahel. J Exp Biol. 2012, 215: 2013-2021. 10.1242/jeb.069468.

Lehmann T, Dao A, Yaro AS, Adamou A, Kassogue Y, Diallo M, Sekou T, Coscaron-Arias C: Aestivation of the African Malaria Mosquito, Anopheles gambiae in the Sahel. AmJTrop Med Hyg. 2010, 83: 601-606. 10.4269/ajtmh.2010.09-0779.

Omer SM, Cloudsley-Thompson JL: Survival of female Anopheles gambiae Giles through a 9-month dry season in Sudan. Bull World Health Organ. 1970, 42: 319-330.

Omer SM, Cloudsley-Thomson JL: Dry season biology of Anopheles gambiae Giles in the Sudan. Nature. 1968, 217: 879-880.

Yaro AS, Traore AI, Huestis DL, Adamou A, Timbine S, Kassogue Y, Diallo M, Dao A, Traore SF, Lehmann T: Dry season reproductive depression of Anopheles gambiae in the Sahel. J Insect Physiol. 2012, 58: 1050-1059. 10.1016/j.jinsphys.2012.04.002.

El-Akad AS, Humphreys JG: Factors Affecting oviposition and egg production in laboratory-reared Anopheles pharoensis Theobald. Bull Soc Vector Ecol. 1988, 13: 243-247.

Xue RD, Ali A, Barnard DR: Effects of forced egg-retention in Aedes albopictus on adult survival and reproduction following application of DEET as an oviposition deterrent. J Vector Ecol. 2005, 30: 45-48.

Wearne HM, Shisler JK: Stressed Versus Unstressed Oviposition Patterns In the Saltmarsh Mosquito, Aedes Sollicitans (Walker), (Diptera: Culicidae). Proc New Jersey Mosq Contr Assoc. 1984, 115-119.

McDonald JL, Lu LC: Viability of mosquito eggs produced by female mosquitoes denied ovipositing sites. Mosq News. 1972, 32: 463-466.

Woke PA: Deferred oviposition in Aedes aegypti (Linn.). Ann Entomol Soc Am. 1955, 48: 39-46.

Yaro AS, Dao A, Adamou A, Crawford JE, Ribeiro JM, Gwadz R, Traore SF, Lehmann T: The distribution of hatching time in Anopheles gambiae. Malaria J. 2006, 5: 19-10.1186/1475-2875-5-19.

Yaro AS, Dao A, Adamou A, Crawford JE, Traore SF, Toure AM, Gwadz R, Lehmann T: Reproductive output of female Anopheles gambiae (Diptera: Culicidae): comparison of molecular forms. J Med Entomol. 2006, 43: 833-839. 10.1603/0022-2585(2006)43[833:ROOFAG]2.0.CO;2.

Holm S: A simple sequentially rejective multiple test procedure. Scand J Stat. 1979, 6: 65-70.

Beier JC: Frequent blood-feeding and restrictive sugar-feeding behavior enhance the malaria vector potential of Anopheles gambiae s.l. and An. funestus (Diptera:Culicidae) in western Kenya. J Med Entomol. 1996, 33: 613-618.

Briegel H, Horler E: Multiple blood meals as a reproductive strategy in Anopheles (Diptera: Culicidae). J Med Entomol. 1993, 30: 975-985.

Smartt CT, Richards SL, Anderson SL, Vitek CJ: Effects of Forced Egg Retention on the Temporal Progression of West Nile Virus Infection in Culex pipiens quinquefasciatus (Diptera: Culicidae). Environ Entomol. 2010, 39: 190-194. 10.1603/EN09172.