Differential Responses of Anopheles stephensi (Diptera: Culicidae) to Skin Emanations of a Man, a Cow, and a Guinea Pig in the Olfactometer
Abstract
Background: Biting habit of mosquitoes plays an important role in the epidemiology of mosquito-borne diseases. Mosquitoes use a set of elaborate sensory modalities to find their preferred hosts by exploiting cues emanating from a nearby host. It has been suggested that the chemical profile of skin can provide further support for anthropophilic mosquito species to find their suitable hosts. This study aimed at revealing the value of skin emanation for a zoo- philic species like Anopheles stephensi as a model.
Methods: Skin emanations of a man, a cow and a Guinea pig were collected by ethanol soaked cottons. Upwind responses of mosquitoes to 100 and 200 3l of filtered skin materials were non-competitively explored in a dual-choice olfactometer. L-lactic acid and other chemical content of the skin samples were identified by an enzymatic kit and GC-MS, respectively.
Results: Unexpectedly, only human skin emanation was resulted in the statistically significant activation and attrac- tion responses of An. stephensi in the wind tunnel. L-lactic acid content of this skin sample was 10 and 29 times more than the cow and the Guinea pig, respectively. The possible role of lactic acid and a few other identified com- pounds have been discussed here.
Conclusion: Anopheles stephensi showed higher and more specific upwind responses to human skin emanation in the olfactometer. Undoubtedly, the thorough explanation of this unexpected finding needs further investigation. But, if new data verify this result, then, it may be necessary to reconsider the role of skin emanation and thence the human blood index and vectorial capacity of this zoophilic mosquito.
Abai MR, Mehravaran A, Vatandoost H, Oshaghi MA, Javadian E, Mashayekhi M, et al. (2008) Comparative performance of imagicides on Anopheles stephensi, main malaria vector in a malarious area, southern Iran. J Vector Borne Dis. 45(4): 307–312.
Acree F, Turner RB, Gouck HK, Beroza M, Smith N (1968) L-Lactic acid: a mos- quito attractant isolated from humans. Science. 161: 1346–1347.
Acree FJ, Beroza M (1962) Quantiative gas chromatography of isomers of insect re- pellent N, N-diethyltoluamide. J Econ En- tomol. 55: 619–622.
Bernier UR, Booth MM, Yost RA (1999) Analysis of human skin emanations by gas chromatography/mass spectrometry. 1. Thermal desorption of attractants for the yellow fever mosquito (Aedes aegypti) from handled glass beads. Anal Chem.71: 1–7.
Bernier UR, Kline DL, Posey HP (2007) Hu- man emanations and related natural com- pounds that inhibit mosquito host finding abilities In: Debboun M, Frances SP and Strickman D (eds.), Insect Repellents: Principles, Methods and Uses. CRC Press Taylor and Francis Group, New York. pp. 77–100.
Bernier UR, Furman KD, Kline DL, Allan SA (2005) Comparison of contact and spatial repellency of catnip oil and N, N- di- ethyl-3-methylbenzamide (Deet) against mosquitoes. J Med Entomol. 42: 306–311.
Bernier UR, Barnard DR, Booth MM, Kline DL, Posey KH, et al. (2004) Chemical composition that attract arthropods, US Patent 6,800,279 B2 October 4 2004. Bosch OJ, Geier M, Boeckh J (2000) Contribution of fatty acids to olfactory host finding of female Aedes aegypti. Chem Senses. 25: 323–330.
Bowen MF (1991) The sensory physiology of host-seeking behaviour in mosquitoes. Annu Rev Entomol. 36: 139–158.
Brady J, Costantini C, Sagnon N, Gibson G, Coluzzi M (1997) The role of body odours in the relative attractiveness of different men to malarial vectors in Burkina Faso. Ann Trop Med Parasitol. 91: S121–S122.
Braks MAH, Anderson RA, Knols BGJ (1999) Infochemicals in mosquito host selection: Human skin micrflora and Plasmodium parasites. Parasitol Today. 15: 409–513.
Braks MAH, Meijerink J, Takken W (2001) The response of the malaria mosquito, Anopheles gambiae, to two components of human sweat, ammonia and L-lactic acid, in an olfactometer. Physiol Entomol. 26: 142–148.
Burkot TR (1988) Non-random host selec- tion by Anopheline mosquitoes. Parasitol Today. 4: 156–162.
Clements AN (1999) The biology of mosqui- toes. Vol. 2. CABI Publishing, New York. Cornel University. pp 130.
Cork A, Park KC (1996) Identification of electrophysiologically-active compounds for the malaria mosquito, Anopheles gam- biae, in human sweat extracts. Med Vet Entomol. 10: 269–276.
Curran AM, Rabin SI, Prada PA, Furton KG (2005) Comparison of the volatile organic compounds present in human odor using SPME-GC/MS. J Chem Ecol. 31: 1607–1619.
Davari B, Vatandoost H, Oshaghi MA, Ladonni H, Enayati AA, Shaeghi M et al. (2007). Selection of Anopheles stephensi with DDT and dieldrin and cross- resis- tance spectrum to pyrethroids and fipronil. Pestic Biochem Physiol. 89(2): 97-103
Dekker T, Steib B, Carde RT, Geier M (2002) L-Lactic acid: a human-signifying host cue for the anthropophilic mosquito Anopheles gambiae. Med Vet Entomol.16: 91–98.
Doosti S, Azari-Hamidian S, Vatandoost H, Oshaghi MA, Hosseini M (2006) Taxo- nomic differentiation of Anopheles sacha- rovi and An.maculipennis S.l. (Diptera: Culicidae) larvae by seta 2 (antepalmate hair). Acta Medica Iranica. 44(1): 21–27.
Doosti S, Vatandoost H, Oshaghi MA, Hosseini M, Sedaghat MM (2007). Applying Mor- phometric Variation of Seta 2 (Antepal- mate Hair) among the Larvae of the Mem- bers of the Maculipennis Sub-group (Dip- tera: Culicidae) in Iran. Iran J Arthropod- Borne Dis. 1(1): 28-37
Enayati AA, Vatandoost H, Ladonni H, Townson H, Hemingway J 2003) Mo- lecular evidence for a Kdr-like pyrethroid resistance mechanism in the malaria vec- tor mosquito Anopheles stephensi. Med Vet Entomol. 17(2): 138–144.
Garrett-Jones C, Boreham PFL, Pant CP (1980) Feeding habits of Anophelines (Dip- tera: Culicidae) in 1971–1978, with refer- ence to the human blood index: a review. Bull Entomol Res. 70: 165–185.
Geier M, Boeckh J (1999) A new Y-tube ol- factometer for mosquitoes to measure the attractiveness of host odours. Entomol Exp Appl. 92: 9–19.
Geier M, Bosch OJ, Boeckh J (1999) Am- monia as an attractive component of host odour for the yellow fever mosquito, Aedes aegypti. Chem Senses. 24: 647–653.
Hanafi-Bojd AA, Vatandoost H, Jafari R (2006) Susceptibility status of An. dthali and An. fluviatilis to commonly used lar- vicides in an endemic focus of malaria, south- ern Iran. J Vector Borne Dis. 43: 34–38.
Hoffman EJ, Miller JR (2002) Reduction of mosquito (Diptera: Culicidae) attacks on a human subject by combination of wind and vapor-phase deet repellent. J Med En- tomol. 39: 935–938.
Kiszewski A, Mellinger A, Spielman A, Ma- laney P, Sachs SE, Sachs J (2004) A global index representing the stability of malaria transmission. Am J Trop Med Hyg 70: 486–498.
Knols BGJ, Meijerink J (1997) Odors influence mosquito behavior. Sci Med. 4: 56–63.
Knols BGJ, de Jong R, Takken W (1995) Differential attractiveness of isolated hu- mans to mosquitoes in Tanzania. Trans R Soc Trop Med Hyg. 89: 604–606.
Koltover VK (2009) Bioantioxidants: the systems reliability standpoint. Toxicol Ind Health. 25: 295–299.
Krishnan KS (1961) Vectors of malaria in India. National Society of India for Malaria and Other Mosquito-borne Disease, Delhi.27–37.
Manouchehri AV, Javadian E, Eshghi N, Motabar M (1976) Ecology of Anopheles stephensi Liston in southern Iran. Trop Geogr Med. 28: 228–232.
Mc Donald G (1958) The epidemiology and control of malaria. Am J Trop Med Hyg.7(5): 577–578
Mc Govern TP, Beroza M, Gouck HK (1967) Chemicals tested as space repellents against yellow-fever mosquitoes, II. Carbanilates, benzamides, aliphatic amides, and imides. J Econ Entomol. 60: 1591–1594.
Naddaf SR, Oshaghi MA, Vatandoost H, Asmar M (2003) Molecular characteriza- tion of the Anopheles fluviatilis species complex in Iran. East Mediterr Health J.9(3): 257–265.
Omrani, SM, Vatandoost H, Oshaghi MA, Shokri F, Guerin PM, Yaaghoobi-Ershadi MR et al (2010) Fabrication of an olfac- tometer for mosquito behavioural studies. J Vector Borne Dis. 47: 17–25.
Pates HV, Takken W, Curtis CF, Huisman PWT, Akinpelu O, Gill GS (2001) Unex- pected anthropophagic behaviour in Ano- pheles quadriannulatus. Med Vet Ento- mol. 15: 293–298.
Price GD, Smith N, Carlson DA (1979) The attraction of female mosquitoes (Anopheles quadrimaculatus Say) to stored human emanations in conjunction with adjusted levels of relative humidity, temperature, and carbon dioxide. J Chem Ecol. 5: 383–395.
Puri SN, Mendki MJ, Sukumaran D, Gane- san K, Prakash S, Sekhar K (2006) Elec- troantennogram and behavioral responses of Culex quinquefasciatus (Diptera: Culici- dae) females to chemicals found in human skin emanations. J Med Entomol. 43: 207–213.
Oshaghi MA, Chavshin AR, Vatandoost H, Yaaghoobi F, Mohtarami, F, Noorjah N (2006a) Effects of postingestion and phy- sical conditions on PCR amplification of host blood meal DNA in mosquitoes. Exp Parasitol. 112: 232–236.
Oshaghi MA, Chavshin AR, Vatandoost H (2006b) Analysis of mosquito bloodmeals using RFLP markers. Exp Parasitol. 114(4):259–264.
Oshaghi MA, Yaghoobi F, Vatandoost H, Abai MR Akbar Zadeh K (2006c) Anopheles stephensi biological forms, geographical distribution, and malaria transmission in malarious regions in Iran. Pak J Biol Sci.9(2): 294–298.
Qiu YT, Smallegange RC, van Loon JJA, Ter Braak CJF, Takken W (2006) Inter- individual variation in the attractiveness of human odours to the malaria mosquito Anopheles gambiae s. s. Med Vet Entomol.20: 280–287.
Reifenrath WG (2005) Natural insect repel- lent. In: Office USPaT (ed.), Washington D.C., U.S. pp 134.
Sastry SD, Buck KT, Janak J, Dressler M, Preti G (1980) Volatiles emitted by hu- mans In: Wiley J (ed.), Biochemical appli- cations of mass spectrometry. Interscience, New York. pp. 1085–1129.
Sedaghat MM, Linton Y-M, Nicolescu G, Smith L, Koliopoulos G, Zounos AK et al (2003a). Morphological and molecular characterization of Anopheles (Anopheles) sacharovi Favre, a primary vector of ma- laria in the Middle East. Systematic Ento- mol. 28: 241–256.
Sedaghat MM, Linton Y-M, Oshaghi MA, Vatandoost H,Harbach RE et al. (2003b) The Anopheles maculipennis complex (Dip- tera: Culicidae) in Iran: molecular charac- terisation and recognition of a new species. Bull Entomol Res. 93: 527–535.
Sedaghat MM, Harbach RE (2005) An anno- tated checklist of the Anopheles mosquitoes (Diptera: Culicidae) in Iran. J Vector Ecol.30: 272–276.
Salari Lak SH, Vatandoost H, Entezarmahdi MR, Ashraf H, Abai MR, Nazari M (2002) Monitoring of insecticide resistance in Ano- pheles sacharovi (Favre, 1903) in border- line of Iran, Armenia, Naxcivan and Turkey,2001. Iran J Pub Health. 31(3-4): 96-99. Skinner WA, Tong H (1965) Repellency of skin-surface lipids of humans to mosqui- toes. Science. 149: 395–306.
Smallegange RC, Qiu YT, Van Loon JA, Tak- ken W (2005) Synergism between am- monia, lactic acid and carboxylic acids as kiromones in the host-seeking behaviour of the malaria mosquito Anopheles gam- biae sensu stricto (Diptera: Culicidae). Chem Senses. 30: 145–152.
Smallegange RC, Qiu YT, Bukovinszkine- Kiss G, Van Loon JJA, Takken W (2009) The effect of aliphatic carboxylic acids on olfaction-based host-seeking of the malaria mosquito Anopheles gambiae sensu stricto. J Chem Ecol. 35: 933–943.
Steib BM, Geier M, Boeckh J (2001) The ef- fect of lactic acid on odour-related host preference of yellow fever mosquitoes. Chem Senses. 26: 523–528.
Takken W (1991) The role of olfaction in host-seeking of mosquitoes: a review. Insect Sci Applic. 12: 287–295.
Takken W, Kline DL (1989) Carbon dioxide and 1-octen-3-ol as mosquito attractants. J Am Mosq Cont Assoc. 5: 311–316.
Takken W and Knols BGJ (1999) Odor-me- diated behaviour of Afrotropical malaria mosquitos. Annu Rev Entomol. 44: 57-131.
Van den Broek IVF, den Otter CJ (1999) Ol factory sensitivities of mosquitoes with dif- ferent host preferences (Anopheles gam-biae s.s., An. arabiensis, An. quadriannulatus, An. m. atroparvus) to synthetic host odors. J Insect Physiol. 45: 1001–1010.
Vatandoost H (2001) Irritability level of Ano- pheles sephensi in Iran. Iran J Public Health. 30 (1-4): 27-30.
Vatandoost H, Moinvaziri VM (2004) Lar- vicidal activity of neem tree extract (Nee- marin) against mosquito larvae in the Is- lamic Republic of Iran. East Mediterr Health J. 10 (4): 573–578.
Vatandoost H, Borhani N (2004) Suscep- tibility and Irritability levels of main ma- laria vectors to synthetic pyrethroids in the endemic areas of Iran. Acta Medica Iranica.42(4): 240–247.
Vatandoost H, Shahi H, Abai MR, Hanafi- Bojd AA, Oshaghi MA, Zamani G (2004) Larval habitats of main malaria vectors in Hormozgan province and their susceptibil- ity to different larvicides. Southeast Asian J Trop Med Pub Hlth. 35: 22–25.
Vatandoost H, Mashayekhi M, Abaie MR, Aflatoonian MR, Hanafi-Bojd AA, Sharifi I (2005a) Monitoring of insecticides re- sistance in main malaria vectors in a ma- larious area of Kahnooj district, Kerman province, southeastern Iran. J Vector Borne Dis. 42: 100–108.
Vatandoost H, Hanafi-Bojd AA (2005b) Cur- rent resistant status of Anopheles stephensi Liston to different larvicides in Hormozgan province, southeastern Iran. Pakistan J Bio Sci. 8: 1568–1570.
Vatandoost H, Gholizadeh MR, Abai MR, Djavadian E (2006a) Laboratory efficacy of protection rate of torn nets treated with pyrethroids, cufluthrin, deltamethrin and permethrin against Anopheles stephensi (Diptera: Culicidae). J Biol Sci. 6(2): 331–336.
Vatandoost H, Oshaghi M, Abaie MR, Shahi M, Yaghoobi F, Baghai M et al. (2006b) Bionomics of Anopheles stephensi Liston in the malarious area of Hormozgan pro- vince, southern Iran. Acta Trop. 97(2):196–205.
Vatandoost H, Ramin E, Rassi Y, Abai MR (2009) Stability and wash resistance of local made mosquito bednets and deter- gents treated with pyrethroids against Ano- pheles stephensi. Iran J Arthropod-Borne Dis .3(1): 19–28.
Vatandoost H, Zahir Nia AH (2010) Respon- siveness of Anopheles maculipennis to different imagicides during resurgent ma- laria. Asia Pac J Trop Med. 3(5):360–363.
Waka M, Hopkins RJ, Glinwood R, Curtis CF (2006) The effect of repellents Ocimum forskolei and deet on the response of Anopheles stephensi to host odours. Med Vet Entomol. 20: 373–376.
Wirtz RA, Turrentine JD, Rutledge LC (1980) Mosquito area repellents: laboratory testing of candidate materials against Aedes ae- gypti. Mosq News. 40: 432–439.
Zahirnia AH, Taherkhani H Vatandoost H (2001) Observation of malaria sporozoite in Anopheles culicifacies (Diptera: Cu- licidae) in Ghasreghand district, Sistan & Baluchistan province. Hakim. 4(2):149–153.
Zahirnia AH, Vatandoost H, Nateghpour M, Javadian E (1998) Insecticide resistance/ susceptibility monitoring in Anopheles pul- cherrimus (Diptera: Culicidae) in Ghasre- ghand district, Sistan and Baluchistan prov- ince, Iran. Hakim. 1: 97–106.
Files | ||
Issue | Vol 4 No 1 (2010) | |
Section | Articles | |
Keywords | ||
Mosquito Host preference Host-seeking An. stephensi Skin emanation Olfactometer |
Rights and permissions | |
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |