In recent years, the East African region has seen an increase in arboviral diseases transmitted by blood-feeding arthropods. Effective surveillance to monitor and reduce incidence of these infections requires the use of appropriate vector sampling tools. Here, trapped skin volatiles on fur from sheep, a known preferred host of mosquito vectors of Rift Valley fever virus (RVFV), were used with a standard CDC light trap to improve catches of mosquito vectors. We tested the standard CDC light trap alone (L), and baited with (a) CO2 (LC), (b) animal volatiles (LF), and (c) CO2 plus animal volatiles (LCF) in two highly endemic areas for RVF in Kenya (Marigat and Ijara districts) from March–June and September–December 2010. The incidence rate ratios (IRR) that mosquito species chose traps baited with treatments (LCF, LC and LF) instead of the control (L) were estimated. Marigat was dominated by secondary vectors and host-seeking mosquitoes were 3–4 times more likely to enter LC and LCF traps [IRR = 3.1 and IRR = 3.8 respectively] than the L only trap. The LCF trap captured a greater number of mosquitoes than the LC trap (IRR = 1.23) although the difference was not significant. Analogous results were observed at Ijara, where species were dominated by key primary and primary RVFV vectors, with 1.6-, 6.5-, and 8.5-fold increases in trap captures recorded in LF, LC and LCF baited traps respectively, relative to the control. These catches all differed significantly from those trapped in L only. Further, there was a significant increase in trap captures in LCF compared to LC (IRR = 1.63). Mosquito species composition and trap counts differed between the RVF sites. However, within each site, catches differed in abundance only and no species preferences were noted in the different baited-traps. Identifying the attractive components present in these natural odors should lead to development of an effective odor-bait trapping system for population density-monitoring and result in improved RVF surveillance especially during the inter-epidemic period.
References
[1]
European Food Safety Authority (EFSA) (2005) Opinion of the Scientific Panel on Animal Health and Welfare (AHAW) on a request from the Commission related to “The Risk of a Rift Valley Fever Incursion and its Persistence within the Community”. Europ Food Safety Auth J 3: 1–128.
[2]
Pepin M, Bouloy M, Bird BH, Kemp A, Paweska (2010) Rift Valley fever virus (Bunyaviridae: Phlebovirus): an update on pathogenesis, molecular epidemiology, vectors, diagnostics and prevention. J Vet Res 41: 61.
[3]
Sang R, Kioko E, Lutomiah J, Warigia M, Ochieng C, et al. (2010) Rift Valley fever virus epidemic in Kenya, 2006/2007: the entomologic investigations. Am J Trop Med Hyg 83 (Suppl 2) 28–37. doi: 10.4269/ajtmh.2010.09-0319
[4]
Gu W, Unnasch TR, Katholi CR, Lampman R, Novak RJ (2008) Fundamental issues in mosquito surveillance for arboviral transmission. Trans R Soc Trop Med Hyg 102: 817–822. doi: 10.1016/j.trstmh.2008.03.019
[5]
Gu W, Novak R (2004) Short report: detection probability of arbovirus infection in mosquito populations. Am J Trop Med Hyg 71: 636–638.
[6]
Takken W (1991) The role of olfaction in host-seeking of mosquitoes: a review. Insect Sci Appl 12: 287–295.
[7]
Davies FG (1975) Observations on the epidemiology of Rift Valley fever in Kenya. J Hyg Camb 75: 219–229. doi: 10.1017/S0022172400047252
[8]
Swanepoel R, Coetzer JAW (2004) Rift Valley fever; Coetzer JA TR, editor. Oxford, UK: Oxford University Press. 1037–1070 p.
[9]
Centers for Disease Control and Prevention (2007) Rift Valley fever outbreak - Kenya, November 2006–January 2007. MWWR 56: 73–76.
[10]
Nguku P, Sharif SK, Mutonga D, Amwayi S, Omollo J, et al. (2010) Investigation of a major outbreak of Rift Valley fever in Kenya, 2006–2007: clues and enigmas concerning Rift Valley fever outbreaks and their prevention. Am J Trop Med Hyg 83: 5–13. doi: 10.4269/ajtmh.2010.09-0288
[11]
Findlay AH, Stephanopoulo GJ, McCallum FO (1936) Presence d'anticorps contre le virus de la fievre de la vallee du Rift dans le sang des africains. Bull Soc Pathol Exot 29: 289–296.
[12]
Traoré-lamizana M, Fontenille D, Diallo M, Ba Y, Zeller HG, et al. (2001) Arbovirus surveillance from 1990 to 1995 in the Barkedji area (Ferlo) of Senegal, a possible natural focus of Rift Valley fever virus. J Med Entomol 38: 480–492. doi: 10.1603/0022-2585-38.4.480
[13]
Zeller HG, Fontenille D, Traore-Lamizana M, Thiongane Y, Digoutte JP (1997) Enzootic activity of Rift Valley fever virus in Senegal. Am J Trop Med Hyg 56: 265–272.
[14]
Edwards FW (1941) Mosquitoes of the Ethiopian region III. Culicine Adults and Pupae. London, UK: British Museum (Nat. Hist.).
[15]
Gillies MT, DeMeillon B (1968) The Anophelinae of Africa South of the Sahara (Ethiopian Zoogeographical region). Johannesburg, South Africa: South African Institute of Medical Research.
[16]
Jupp PG (1996) Mosquitoes of Southern Africa: Culicinae and Toxorhynchitinae. Hartebeespoort, South Africa: Ekogilde Publishers.
[17]
R Development Core Team (2010) R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria.
[18]
Omondi D (2011) Molecular screening of mosquitoes and their blood meals for Rift Valley fever and vertebrate host identification. Masters Thesis to the Graduate School: Egerton University. 74 p.
[19]
Lawrence BR (1960) The biology of two species of mosquito Mansonia africana (Theobald) and Mansonia uniformis (Theobald), belonging to the subgenus Mansonioides (Diptera, Culicidae). Bull Entomol Res 51: 491–517. doi: 10.1017/s0007485300055127
[20]
Hayes RO, Templis CH, Hess AD, Reeves WC (1973) Mosquito host preference studies in Hale County, Texas. Am J Trop Med Hyg 22: 270–277.
[21]
Reisen WK, Pfuntner SR, Milby MM, Templis CH, Presser SB (1990) Mosquito bionomics and the lack of arbovirus activity in the Chino area of San Bernardino County, California. J Med Entomol 27: 811–818.
[22]
Torr SJ, Della Torre A, Calzetta M, Costantini C, Vale GA (2008) Towards a fuller understanding of mosquito behaviour: use of electrocuting grids to compare the Odor orientated responses of Anopheles arabiensis and An. quadriannulatus in the field. Med Vet Entomol 22: 93–108. doi: 10.1111/j.1365-2915.2008.00723.x
[23]
Mukabana WR, Takken W, Killeen GF, Knols BGJ (2004) Allomonal effect of breath contributes to differential attractiveness of humans to the African malaria vector Anopheles gambiae. Malar J 3: 1. doi: 10.1186/1475-2875-3-1
[24]
Takken W, Kline D (1989) Carbon dioxide and 1-octen-3-ol as mosquito attractants. J Am Mosq Control Assoc 5: 311–316.
[25]
Dekker T, Geier M, Cardé RT (2005) Carbon dioxide instantly sensitizes female yellow fever mosquitoes to human skin odours. J Exp Biol 208: 2963–2972. doi: 10.1242/jeb.01736
[26]
Spitzen J, Smallegange RC, Takken W (2008) Effect of human odors and positioning of CO2 release point on trap catches of the malaria mosquito Anopheles gambiae sensu stricto in an olfactometer. Physiol Entomol 33: 116–122. doi: 10.1111/j.1365-3032.2008.00612.x
[27]
Allan SA, Bernier UR, Kline DL (2006) Laboratory evaluation of avian odors for mosquito (Diptera: Culicidae) attraction. J Med Entomol 43: 225–231. doi: 10.1603/0022-2585(2006)043[0225:LEOAOF]2.0.CO;2
[28]
Syed Z, Leal W (2009) Acute olfactory response of Culex mosquitoes to a human- and bird-derived attractant. Proc Natl Acad Sci USA 106: 18803–18808. doi: 10.1073/pnas.0906932106
[29]
Allan SA, Day JF, Edman JD (1987) Visual ecology of biting flies. Annu Rev Entomol 32: 297–316. doi: 10.1146/annurev.en.32.010187.001501
[30]
Qiu YT, Spitzen J, Smallegange RC, Knols BGJ (2007) Monitoring systems for adult insect pests and disease vectors. In: Takken W, Knols B, editors. Emerging Pests and Vector-borne Diseases in Europe. Wageningen: Wageningen Academic Publishers pp. 329–354.
[31]
Kawada H, Takemura S, Arikawa K, Takagi M (2005) Comparative study on nocturnal behavior of Aedes aegypti and Aedes albopictus. J Med Entomol 42: 312–318. doi: 10.1603/0022-2585(2005)042[0312:CSONBO]2.0.CO;2
[32]
Dekker T, Steib B, Cardé RT, Geier M (2002) L-Lactic acid: a human-signifying host cue for the anthropophilic mosquito Anopheles gambiae. Med Vet Entomol 16: 91–98. doi: 10.1046/j.0269-283x.2002.00345.x
[33]
Mboera LEG, Takken W (1997) Carbon dioxide chemotropism in mosquitoes (Diptera: Culicidae) and its potential in vector surveillance and control. Rev Med Vet Entomol 85: 355–368.
[34]
Olanga EA, Okal MN, Mbadi PA, Kokwaro ED, Mukabana WR (2010) Attraction of Anopheles gambiae to odor baits augmented with heat and moisture. Malar J 9: 6. doi: 10.1186/1475-2875-9-6
[35]
Birkett MA, Agelopoulos N, Jensen MV, Jespersen JB, Pickett JA, et al. (2004) The role of volatile semiochemicals in mediating host location and selection by nuisance and disease-transmitting cattle flies. Med Vet Entomol 18: 313–322. doi: 10.1111/j.0269-283X.2004.00528.x
[36]
Logan JG, Birkett M (2007) Review: Semiochemicals for biting fly control: their identification and exploitation. Pest Manag Sci 63: 647–657. doi: 10.1002/ps.1408
[37]
Gillies M (1980) The role of carbon dioxide in host-finding by mosquitoes: a review. Bull Entomol Res 70: 525–532. doi: 10.1017/s0007485300007811
[38]
Clements AN (1999) The biology of mosquitoes. New York: CABI.
[39]
Costantini C, Sagnon N, Della Torre A, Diallo M, Brady J, et al. (1998) Odor-mediated host preferences of West African mosquitoes, with particular reference to malaria vectors. Am J Trop Med Hyg 58: 56–63. doi: 10.1017/s0007485300007811
[40]
Duchemin JB, Leongpocktsy JM, Rabarison P, Roux J, Coluzzi M, et al. (2001) Zoophily of Anopheles arabiensis and An. gambiae in Madagascar demonstrated by odor-baited entry traps. Med Vet Entomol 15: 50–57. doi: 10.1046/j.1365-2915.2001.00276.x
[41]
Kilpatrick AM, Kramer LD, Jones MJ, Marra PP, Daszak P (2006) West Nile virus epidemics in North America are driven by shifts in mosquito feeding behavior. PLoS Biol 4: e82. doi: 10.1371/journal.pbio.0040082
[42]
Williams CR, Kokkinn MJ, Smith BP (2003) Intraspecific variation in odor-mediated host preference of the mosquito Culex annulirostris. J Chem Ecol 29: 1889–1903. doi: 10.1023/A:1024806429366
[43]
Van Den Hurk AF, Montgomery BL, Zborowski P, Beebe NW, Cooper RD, et al. (2006) Does 1-octen-3-ol enhance trap collections of Japanese encephalitis virus mosquito vectors in northern Australia? J Am Mosq Control Assoc 22: 15–21. doi: 10.2987/8756-971X(2006)22[15:DOETCO]2.0.CO;2
[44]
Cooperband MF, McElfresh JS, Millar JG, Carde RT (2008) Attraction of female Culex quinquefasciatus Say (Diptera: Culicidae) to odors from chicken feces. J Insect Physiol 54: 1184–1192. doi: 10.1016/j.jinsphys.2008.05.003
[45]
Mohamed-Ahmed MM, Abdulla MA, Mohamed YO, El Rayah IE, El Amin YE (2007) Trapability of periurban populations of horseflies (Diptera: Tabanidae) in Khartoum State, Sudan. J Sci Technol 8: 46–63.
[46]
Mihok S, Mulye H (2010) Responses of tabanids to Nzi traps baited with octenol, cow urine and phenols in Canada. Med Vet Entomol 24 (3) 266–272. doi: 10.1111/j.1365-2915.2010.00889.x
[47]
Lambrechts L, Knox TB, Wong J, Liebman KA, Albright RG, et al. (2009) Shifting priorities in vector biology to improve control of vector-borne disease. Trop Med Int Hlth 14: 1505–1514.
[48]
Mands V, Kline DL, Blackwell A (2004) Culicoides midge trap enhancement with animal odor baits in Scotland. Med Vet Entomol 18: 336–342. doi: 10.1111/j.0269-283X.2004.00516.x
[49]
Njiru BN, Mukabana WR, Takken W, Knols BGJ (2006) Trapping of the malaria vector Anopheles gambiae with odor-baited MM-X traps in semi-field conditions in western Kenya. Malar J 5: 39. doi: 10.1186/1475-2875-5-39
[50]
Jawara M, Smallegange RC, Jeffries D, Nwakanma DC, Awolola TS, et al. (2010) Optimizing odor-baited trap methods for collecting mosquitoes during the malaria season in The Gambia. PLoS ONE 4: e8167. doi: 10.1371/journal.pone.0008167
[51]
Gillies MT, Wilkes T (1968) A comparison of the range of attraction of animal baits and of carbon dioxide for some West African mosquitoes. Bull Entomol Res 59: 441–456. doi: 10.1017/S0007485300003412
[52]
Bernier UR, Kline D, Barnard DR, Shreck CE, Yost RA (2000) Analysis of human skin emanations by gas chromatography/mass spectrometry. 2 Identification of volatile compounds that are candidate attractants for yellow fever mosquito (Aedes aegypti) Analytical Chem 72: 747–756. doi: 10.1021/ac990963k
[53]
Qiu YT, Smallegange RC, Van Loon JJ, Ter Braak CJ, Takken W (2006) Interindividual variation in the attractiveness of human odours to the malaria mosquito Anopheles gambiae s. s. Med Vet Entomol 20: 280–287. doi: 10.1111/j.1365-2915.2006.00627.x