Identification of Cattle-Derived Volatiles that Modulate the Behavioral Response of the Biting Midge Culicoides nubeculosus
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Abstract
Identification of host-derived volatiles is an important step towards the development of novel surveillance and control tools for Culicoides biting midges. In this study, we identified compounds from headspace collections of cattle hair and urine that modulate the behavioral response of Culicoides nubeculosus, a research model species with a similar host-range as the vectors of Bluetongue disease and Schmallenberg disease in Europe. Combined gas chromatography and electroantennographic detection (GC-EAD) analysis revealed 23 bioactive compounds, of which 17, together with octanal, were evaluated in a two-choice behavioral assay in the presence of CO2. Decanal, 2-phenylethanal, 1-octen-3-ol, 2-ethylhexanol, 3-methylindole, phenol, and 3-ethylphenol elicited attraction of host seeking C. nubeculosus, whereas heptanal, octanal, nonanal, 3-propylphenol, and 4-propylphenol inhibited the insects’ attraction to CO2, when compared to CO2 alone. 6-Methyl-5-hepten-2-one, 3-methylphenol, 4-methylphenol, and 4-ethylphenol elicited both attraction and inhibition. The behavioral responses were dependent on the concentration tested. Our results show that cattle-derived odors have the potential to be used for the manipulation of the behavior of Culicoides biting midges.
Keywords
Culicoides nubeculosus Attraction Behavioral inhibition Bluetongue Schmallenberg Diptera CeratopogonidaeNotes
Acknowledgments
This project was financed by the Swedish Research Council (Formas) and supported by the Linnaeus Grant IC-E3 (Formas, Sweden). DPB is supported by an EU Intra-European Fellowship. The authors would also like to acknowledge Simon Carpenter, Eric Denison and James Barber at The Pirbright Institute for their generous supply of C. nubeculosus.
Compliance with Ethical Standards
Conflict of Interest
The authors declare that they have no conflict of interest.
References
- Arn H (1975) The electroantennographic detector — a selective and sensitive tool in the gas chromatographic analysis of insect pheromones. Z Naturforsch 30:722–725Google Scholar
- Beer M, Conraths FJ, Van der Poel WHM (2013) 'Schmallenberg virus' - a novel orthobunyavirus emerging in Europe. Epidemiol Infect 141:1–8CrossRefPubMedGoogle Scholar
- Bhasin A, Mordue AJ, Mordue W (2000) Electrophysiological and behavioural identification of host kairomones as olfactory cues for Culicoides impunctatus and C. nubeculosus. Physiol Entomol 25:6–16CrossRefGoogle Scholar
- Bhasin A, Mordue AJ, Mordue W (2001) Field studies on efficacy of host odour baits for the biting midge Culicoides impunctatus in Scotland. Med Vet Entomol 15:147–156CrossRefPubMedGoogle Scholar
- Birkett MA, Agelopoulos N, Jensen KMV, Jespersen JB, Pickett JA, Prijs HJ, Thomas G, Trapman JJ, Wadhams LJ, Woodcock CM (2004) The role of volatile semiochemicals in mediating host location and selection by nuisance and disease-transmitting cattle flies. Med Vet Entomol 18:313–322CrossRefPubMedGoogle Scholar
- Bjostad L (1998) Electrophysiological methods. Kluwer Academic Publishing, Dordrecht, NetherlandsCrossRefGoogle Scholar
- Blackwell A, Luntz AJM, Mordue W (1992) Morphology of the antennae of 2 species of biting midge – Culicoides impunctatus (goetghebuer) and Culicoides nubeculosus (Meigen) (Diptera, Ceratopogonidae). J Morphol 213:85–103CrossRefPubMedGoogle Scholar
- Blackwell A, Brown M, Mordue W (1995) The use of an enhanced ELISA method for the identification of Culicoides bloodmeals in host-preference studies. Med Vet Entomol 9:214–218CrossRefPubMedGoogle Scholar
- Blackwell A, Dyer C, Mordue AJ, Wadhams LJ, Mordue W (1996) The role of 1-octen-3-ol as a host-odour attractant for the biting midge, Culicoides impunctatus Goetghebuer, and interactions of 1-octen-3-ol with a volatile pheromone produced by parous female midges. Physiol Entomol 21:15–19CrossRefGoogle Scholar
- Bruce T, Pickett J (2011) Perception of plant volatile blends by herbivorous insects - Finding the right mix. Phytochemistry 72:1605–1611CrossRefPubMedGoogle Scholar
- Bursell E, Gough AJE, Beevor PS, Cork A, Hall DR, Vale GA (1988) Identification of components of cattle urine attractive to tsetse flies, Glossina spp (Diptera, Glossinidae). Bull Entomol Res 78:281–291CrossRefGoogle Scholar
- Caracappa S, Torina A, Guercio A, Vitale F, Calabro A, Purpari G, Ferrantelli V, Vitale M, Mellor PS (2003) Identification of a novel bluetongue virus vector species of Culicoides in Sicily. Vet Rec 153:71–74CrossRefPubMedGoogle Scholar
- Carpenter S, Mellor PS, Torr SJ (2008) Control techniques for Culicoides biting midges and their application in the UK and northwestern Palaearctic. Med Vet Entomol 22:175–187CrossRefPubMedGoogle Scholar
- Carpenter S, Wilson A, Mellor PS (2009) Culicoides and the emergence of bluetongue virus in northern Europe. Trends Microbiol 17:172–178CrossRefPubMedGoogle Scholar
- Cilek JE, Kline DL, Hallmon CF (2003) Evaluation of a novel removal trap system to reduce biting midge (Diptera : Ceratopogonidae) populations in Florida backyards. J Vector Ecol 28:23–30PubMedGoogle Scholar
- den Otter CJ (1991) Olfactory responses of tsetse-flies to phenols from buffalo urine. Physiol Entomol 16:401–410CrossRefGoogle Scholar
- den Otter CJ, Tchicaya T, Vandenberg MJ (1988) Olfactory sensitivity of 5 species of tsetse (Glossina spp) to 1-octen-3-ol, 4-heptanone, 3-nonanone and acetone. Insect Sci Appl 9:213–218Google Scholar
- Dijkstra E, van der Ven IJK, Melswinkel R, Holzel DR, van Rijn PA, Meiswinkel R (2008) Culicoides chiopterus as a potential vector of bluetongue virus in Europe. Vet Rec 162:424–424CrossRefGoogle Scholar
- Gerry AC, Monteys VSI, Vidal JOM, Francino O, Mullens BA (2009) Biting rates of Culicoides midges (Diptera: Ceratopogonidae) on sheep in northeastern Spain in relation to midge capture using UV light and carbon dioxide-baited traps. J Med Entomol 46:615–624CrossRefPubMedGoogle Scholar
- Ghaninia M, Larsson M, Hansson BS, Ignell R (2008) Natural odor ligands for olfactory receptor neurons of the female mosquito Aedes aegypti: Use of gas chromatography-linked single sensillum recordings. J Exp Biol 211:3020–3027CrossRefPubMedGoogle Scholar
- Gikonyo NK, Hassanali A, Njagi PGN, Gitu PM, Midiwo JO (2002) Odor composition of preferred (buffalo and ox) and nonpreferred (waterbuck) hosts of some savanna tsetse flies. J Chem Ecol 28:969–981CrossRefPubMedGoogle Scholar
- Gikonyo NK, Hassanali A, Njagi PGN, Saini RK (2003) Responses of Glossina morsitans morsitans to blends of electroantennographically active compounds in the odors of its preferred (buffalo and ox) and nonpreferred (waterbuck) hosts. J Chem Ecol 29:2331–2345CrossRefPubMedGoogle Scholar
- Guerenstein PG, Guerin PM (2001) Olfactory and behavioural responses of the blood-sucking bug Triatoma infestans to odours of vertebrate hosts. J Exp Biol 204:585–597PubMedGoogle Scholar
- Guidobaldi F, Guerenstein PG (2013) Evaluation of a CO2-free commercial mosquito attractant to capture triatomines, vectors of Chagas disease, in the laboratory. J Vector Ecol 38:245–250CrossRefPubMedGoogle Scholar
- Hall DR, Beevor PS, Cork A, Nesbitt BF, Vale GA (1984) 1-octen-3-ol - a potent olfactory stimulant and attractant for tsetse isolated from cattle odors. Insect Sci Appl 5:335–339Google Scholar
- Harraca V, Ryne C, Birgersson G, Ignell R (2012) Smelling your way to food: Can bed bugs use our odour? J Exp Biol 215:623–629CrossRefPubMedGoogle Scholar
- Harrup LE, Logan JG, Cook JI, Golding N, Birkett MA, Pickett JA, Sanders S, Berber J, Rogers DJ, Mellor PS, Purse BV, Carpenter S (2012) Collection of Culicoides (Diptera: Ceratopogonidae) using CO2 and enantiomers of 1-octen-3-ol in the United Kingdom. J Med Entomol 49:112–121CrossRefPubMedGoogle Scholar
- Hill SR, Hansson BS, Ignell R (2009) Characterization of antennal trichoid sensilla from female Southern house mosquito, Culex quinquefasciatus Say. Chem Senses 34:231–252CrossRefPubMedGoogle Scholar
- Jennings DM, Mellor PS (1988) The vector potential of British Culicoides species for Bluetongue virus. Vet Microbiol 17:1–10CrossRefPubMedGoogle Scholar
- Kettle DS (1962) Bionomics and control of Culicoides and Leptoconops - (Diptera, Ceratopogonidae, Heleidae). Annu Rev Entomol 7:401–418CrossRefGoogle Scholar
- Kline DL, Hagan DV, Wood JR (1994) Culicoides responses to 1-octen-3-ol and carbon dioxide in salt marshes near Sea island, Georgia, USA. Med Vet Entomol 8:25–30CrossRefPubMedGoogle Scholar
- Kline DL, Takken W, Wood JR, Carlson DA (1990) Field studies on the potential of butanone, carbon-dioxide, honey extract, 1-octen-3-ol, l-lactic acid and phenols as attractants for mosquitos. Med Vet Entomol 4:383–391CrossRefPubMedGoogle Scholar
- Lassen SB, Nielsen SA, Skovgard H, Kristensen M (2011) Molecular identification of bloodmeals from biting midges (Diptera: Ceratopogonidae: Culicoides Latreille) in Denmark. Parasitol Res 108:823–829CrossRefPubMedGoogle Scholar
- Logan JG, Birkett MA (2007) Semiochemicals for biting fly control: their identification and exploitation. Pest Manag Sci 63:647–657CrossRefPubMedGoogle Scholar
- Logan JG, Birkett MA, Clark SJ, Powers S, Seal NJ, Wadhams LJ, Mordue AJ, Pickett JA (2008) Identification of human-derived volatile chemicals that interfere with attraction of Aedes aegypti mosquitoes. J Chem Ecol 34:308–322CrossRefPubMedGoogle Scholar
- Logan JG, Seal NJ, Cook JI, Stanczyk NM, Birkett MA, Clark SJ, Gezan SA, Wadhams LJ, Pickett JA, Mordue AJ (2009) Identification of human-derived volatile chemicals that interfere with attraction of the Scottish biting midge and their potential use as repellents. J Med Entomol 46:208–219CrossRefPubMedGoogle Scholar
- Mair J, Blackwell A (1996) Mating behavior of Culicoides nubeculosus (Diptera: Ceratopogonidae). J Med Entomol 33:856–858CrossRefPubMedGoogle Scholar
- Mands V, Kline DL, Blackwell A (2004) Culicoides midge trap enhancement with animal odour baits in Scotland. Med Vet Entomol 18:336–342CrossRefPubMedGoogle Scholar
- Meiswinkel R, van Rijn P, Leijs P, Goffredo M (2007) Potential new Culicoides vector of bluetongue virus in northern Europe. Vet Rec 161:564–565CrossRefPubMedGoogle Scholar
- Mellor PS (2000) Replication of arboviruses in insect vectors. J Comp Pathol 123:231–247CrossRefPubMedGoogle Scholar
- Mellor PS, McCaig J (1974) Probable cause of Sweet-itch in England. Vet Rec 95:411–415CrossRefPubMedGoogle Scholar
- Nielsen BO, Christensen O (1975) Mass attack by biting midge Culicoides nubeculosus (mg) (Dipteria, Ceratopogonidae) on grazing cattle in Denmark - New aspect of sewage discharge. Nord Vet Med 27:365–372PubMedGoogle Scholar
- Pettersson E, Bensch S, Ander M, Chirico J, Sigvald R, Ignell R (2012) Molecular identification of blood meals and species composition in Culicoides biting midges. Med Vet Entomol 27:104–112CrossRefPubMedGoogle Scholar
- Pickett JA, Birkett MA, Dewhirst SY, Logan JG, Omolo MO, Torto B, Pelletier J, Syed Z, Leal WS (2010) Chemical ecology of animal and human pathogen vectors in a changing global climate. J Chem Ecol 36:113–121CrossRefPubMedGoogle Scholar
- Qiu YT, van Loon JJA, Takken W, Meijerink J, Smid HM (2006) Olfactory coding in antennal neurons of the malaria mosquito, Anopheles gambiae. Chem Senses 31:845–863CrossRefPubMedGoogle Scholar
- Rasmussen LD, Kristensen B, Kirkeby C, Rasmussen TB, Belsham GJ, Bodker R, Botner A (2012) Culicoids as vectors of Schmallenberg virus. Emerg Infect Dis 18:1204–1206PubMedCentralCrossRefPubMedGoogle Scholar
- R Core Team (2014) R: A language and environment for statistical computing. 416 Vienna, Austria R foundation for statistical computingGoogle Scholar
- Ritchie SA, Vanessen PHA, Kemme JA, Kay BH, Allaway D (1994) Response of biting midges (Diptera, Ceratopogonidae) to carbon dioxide, octenol, and light in southeastern Queensland, Australia. J Med Entomol 31:645–648CrossRefPubMedGoogle Scholar
- Savini G, MacLaclalan NJ, Sanchez-Vinaino JM, Zientara S (2008) Vaccines against bluetongue in Europe. Comp Immunol Microb 31:101–120CrossRefGoogle Scholar
- Siju KP, Hill SR, Hansson BS, Ignell R (2010) Influence of blood meal on the responsiveness of olfactory receptor neurons in antennal sensilla trichodea of the yellow fever mosquito, Aedes aegypti. J Insect Physiol 56:659–665CrossRefPubMedGoogle Scholar
- Syed Z, Leal WS (2009) Acute olfactory response of Culex mosquitoes to a human- and bird-derived attractant. Proc Natl Acad Sci U S A 106:18809–18814CrossRefGoogle Scholar
- Takken W, Kline DL (1989) Carbon-dioxide and 1-octen-3-ol as mosquito attractants. J Am Mosq Control Assoc 5:311–316PubMedGoogle Scholar
- Tchouassi DP, Sang R, Sole CL, Bastos ADS, Teal PEA, Borgemeister C, Torto B (2013) Common host-derived chemicals increase catches of disease-transmitting mosquitoes and can improve early warning systems for Rift valley fever virus. Plos Negl Trop Dis 7:e2007PubMedCentralCrossRefPubMedGoogle Scholar
- Thorat T, Yadav V, Yadav G (1992) Esterification of phthalic-anhydride with 2-ethylhexanol by solid superacidic catalysts. Appl Catal A-Gen 90:73–96CrossRefGoogle Scholar
- Torr SJ, Hall DR, Smith JL (1995) Responses of tsetse-flies (Diptera, Glossinidae) to natural and synthetic ox odors. Bull Entomol Res 85:157–166CrossRefGoogle Scholar
- Vale G, Torr S (2004) Development of bait technology to control tsetse. The Trapanosomiases, ed by Maudlin I, et al CABI Publishing:509–523Google Scholar
- Vale GA, Hall DR, Gough AJE (1988) The olfactory responses of tsetse flies, Glossina spp (Diptera, Glossinidae), to phenols and urine in the field. Bull Entomol Res 78:293–300CrossRefGoogle Scholar
- Venter GJ, Labuschagne K, Boikanyo SNB, Majatladi DM, Morey L (2011) The effect of 1-octen-3-ol and 4-methylphenol on Culicoides midge numbers collected with suction light traps in South Africa. Vet Parasitol 175:182–186CrossRefPubMedGoogle Scholar
- Veronesi E, Antony F, Gubbins S, Golding N, Blackwell A, Mertens PPC, Brownlie J, Darpel KE, Mellor PS, Carpenter S (2013a) Measurement of the infection and dissemination of bluetongue virus in Culicoides biting midges using a semi-quantitative RT-PCR assay and isolation of infectious virus. Plos One 8:e70800PubMedCentralCrossRefPubMedGoogle Scholar
- Veronesi E, Henstock H, Gubbins S, Batten C, Manley R, Barber J, Hoffmann B, Beer M, Attoui H, Mertens PPC, Carpenter S (2013b) Implicating Culicoides biting midges as vectors of Schmallenberg virus using Semi-Quantitative RT-PCR. Plos One 8:e57747PubMedCentralCrossRefPubMedGoogle Scholar
- Viennet E, Garros C, Lancelot R, Allène X, Gardès L, Rakotoarivony I, Crochet D, Delécolle JC, Moulia C, Baldet T, Balenghien T (2011) Assessment of vector/host contact: Comparison of animal-baited traps and UV-light/suction trap for collecting Culicoides biting midges (Diptera: Ceratopogonidae), vectors of Orbiviruses. Parasite Vector 4:119CrossRefGoogle Scholar