Chemical Ecology Group

Semiochemicals mediating interactions with blood feeding (haematophagous) insects

Mosquito feeding

The Chemical Ecology Group at Rothamsted has been identifying semiochemicals for arthropod pests of medical and veterinary importance since the early 1980’s, when we first identified the Culex quinquefasciatus oviposition pheromone (Figure 1). Today, a substantial proportion of the group research is focussed on investigating semiochemicals that can be exploited to improve or develop monitoring and control strategies for many haematophagous (blood-feeding) pests affecting human and livestock health and welfare (See box 1). These include the malaria mosquito, Anopheles gambiae and the tsetse fly, Glossina spp. which spreads African sleeping sickness (trypanosomiasis). Our multidisciplinary approach allows us to isolate and identify new semiochemicals and provide a better understanding of their role through insect behaviour studies, analytical chemistry, sophisticated electrophysiology techniques (Figure 2) and molecular biology. Using these methods, we have investigated various semiochemicals that are used during the location of a suitable host (kairomones and allomones), a breeding site (oviposition pheromones) or a mate (sex and aggregation pheromones).

Haematophagous arthropods show differential attraction towards certain host species, and even towards specific individuals within a species. This was initially demonstrated in our group for cattle flies, e.g. the horn fly, Haematobia irritans (Diptera: Muscidae) that feed preferentially on individual heifers, where differential fly-loads were shown to be mediated by the production of repellents, such as 6-methyl-5-hepten-2-one, by the unattractive heifers (Figure 2). Most recently, we have demonstrated that, for human beings, the same mechanism for low attractiveness to mosquitoes and midges is caused by the production of similar repellent compounds (Figure 3). This work was showcased at the Royal Society Summer Science Exhibition in London and Glasgow and at the Queen's Science Day at Buckingham Palace. The compounds identified in this study are currently being developed as natural repellents against biting insects. We have also shown that host preference and non-host avoidance by arthropods within the marine environment is also mediated by volatile semiochemicals, with kairomones identified for the parasitic sealice species, Lepeoptheirus salmonis and Calagus rogercresseyi, which are major pests of salmonid aquaculture.

As well as studying host-arthropod interactions, we are also investigating semiochemicals that play a role in other aspects of pest arthropod biology. These include:

• Male-produced sex pheromones, 9-methylgermacrene-B and 3-methyl-α-himachalene for Brazilian populations of the sandfly, Lutzomyia longipalpis (Figure 1)
• Aggregation pheromones for the American and European House Dust Mite, Dermatophagoides farinae and D. pteromyssinus, the Red Poultry Mite, Dermanyssus gallinae, and bedbugs, Cimex lectularius
• A female-produced sex pheromone for the farmyard biting midge, Culicoides nebeculosus
• Sex pheromones for the sealice species, L. salmonis and C. rogercresseyi
• Oviposition site cues for Aedes spp and Culex spp. mosquitoes

By combining attractants and repellents, we aim to develop provide a "push-pull" control strategy for arthropod pest control, whereby repellents would be used to "push" pests away and attractants would be used to "pull" pests into traps.

Wherever possible, once semiochemicals have been identified, we aim to develop novel pest control strategies that utilise renewable resources for semiochemical production. For haematophagous arthropods, this is exemplified by the production of the Culex spp. oviposition pheromone and L. longipalpis sex pheromones from Kochia scoparia and Geranium macrorrhizum fixed and essential oils respectively (see web-link "A Green Chemistry Approach for Insect Semiochemical Production")

We are always extremely keen to cooperate with other people in the field of medical and veterinary entomology/chemical ecology and welcome any potential collaborators.

Mosquitoes (Diptera: Culicidae)	Anopheles spp.; Aedes spp.; Culex spp.
Midges (Diptera: Ceratopogonidae)	Culicoides spp.
Tsetse flies (Diptera: Glossinidae)	Glossina spp.
Cattle flies (Diptera: Muscidae)	Haematobia spp. Stomoxys spp.
Sandflies (Diptera: Psychodidae)	Lutzomyia longipalpis
Bedbugs (Hemiptera: Cimicidae)	Cimex lecturalius
House Dust Mites (Acari: Pyroglyphidae)	Dermatophagoides farinae and D. pteromyssinus
Red Poultry Mites (Acari: Dermanyssidae)	Dermanyssus gallinae
Sealice (Copepoda: Caligidae)	Lepeoptheirus salmonis and Calagus rogercresseyi
Box 1. Medically and veterinary important arthropods that are investigated in the Chemical Ecology group at Rothamsted Research

Relevant Publications

Host-arthropod interactions

C. Costantini, M.A. Birkett, G. Gibson, J. Ziesmann, N'F. Sagnon, H.A. Mohammed, M. Coluzzi and J.A. Pickett (2001). Electroantennogram and behavioural responses of the malaria vector Anopheles gambiae to human-specific sweat components. Medical and Veterinary Entomology 15, 259-266.

Birkett, M.A. Towards an organic system for cattle fly control: a push and a pull? 2004. Proceedings Joint BGS/AAB/COR conference “Organic Farming – Science and Practice for Profitable Livestock Production”, 20-22 April 2004.

Jensen, K-M.V., Jespersen, J.B., Birkett, M.A., Pickett, J.A., Thomas, G., Wadhams, L.J., and Woodcock, C.M. (2004). Variation in the load of the horn fly, Haematobia irritans (L.), (Diptera: Muscidae) in cattle herds is determined by the presence or absence of individual heifers. Medical and Veterinary Entomology, 18, 275-280.

Birkett, M.A., Agelopoulos, N., Jensen, K-M.V., Jespersen, J.B., Pickett, J.A., Pickett, J.A, Prijs., Thomas, G., Trapman, J.J., Wadhams, L.J., and Woodcock, C.M. (2004). The role of volatile semiochemicals in mediating host location and selection by nuisance and disease-transmitting cattle flies. Medical and Veterinary Entomology, 18, 313-322.

G.J. Devine, A. Ingvarsdóttir, W. Mordue, A.W. Pike, J.A. Pickett, I. Duce and A.J. Mordue (Luntz) (2000) Salmon lice, Lepeophtheirus salmonis, exhibit specific chemotactic responses to semiochemicals originating from the salmonid, Salmo salar. Journal of Chemical Ecology 26, 1833-1847.

A.Ingvarsdottir, M.A. Birkett, I. Duce, R. Genna, W. Mordue, J. Pickett, L. Wadhams and A.J. Mordue (Luntz) (2002). Semiochemical strategies for sea lice control: host location cues. Pest Management Science, 58, 6, 537-545.

Bailey, R.A., Birkett, M.A., Ingvarsdottir, A., Mordue Luntz, A.J., Mordue, W., Pickett, J.A. and Wadhams, L.J. (2006). The role of semiochemicals in mediating host location and non-host avoidance by copepodid larvae of the parasitic sea louse, Lepeoptheirus salmonis, Canadian Journal of Fisheries and Aquatic Sciences, 63, 448-456.

Pheromones/Oviposition cues

B.R. Laurence and J.A. Pickett (1982). Erythro-6-Acetoxy-5-hexadecanolide, the major component of a mosquito oviposition attractant pheromone. Journal of the Chemical Society Chemical Communications, 59–60.

B.R. Laurence, K. Mori, T. Otsuka, J.A. Pickett and L.J. Wadhams (1985) Absolute configuration of mosquito oviposition attractant pheromone, 6–acetoxy–5–hexadecanolide. Journal of Chemical Ecology 11, 643–648.

B.R. Laurence and J.A. Pickett (1985) An oviposition attractant pheromone in Culex quinquefasciatus Say (Diptera: Culicidae). Bulletin of Entomological Research 75, 283–290.

W.A. Otieno, T.O. Onyango, M.M. Pile, B.R. Laurence, G.W. Dawson, L.J. Wadhams and J.A. Pickett (1988) A field trial of the synthetic oviposition pheromone with Culex quinquefasciatus Say (Diptera: Culicidae) in Kenya. Bulletin of Entomological Research 78, 463–470.

G.W. Dawson, B.R. Laurence, J.A. Pickett, M.M. Pile and L.J. Wadhams (1989) A note on the mosquito oviposition pheromone. Pesticide Science 27, 277–280.

G.W. Dawson, A. Mudd, J.A. Pickett, M.M. Pile and L.J. Wadhams (1990) Convenient synthesis of mosquito oviposition pheromone and a highly fluorinated analog retaining biological activity. Journal of Chemical Ecology 16, 1779-1789.

A.J. Mordue (Luntz), A. Blackwell, B.S. Hansson, L.J. Wadhams and J.A. Pickett (1992) Behavioural and electrophysiological evaluation of oviposition attractants for Culex quinquefasciatus Say (Diptera: Culicidae). Experientia 48, 1109-1111.

A.J. Mordue (Luntz), A. Blackwell, B.S. Hansson, L.J. Wadhams and J.A. Pickett (1993) Oviposition attractants for Culex quinquefasciatus. IOBC/WPRS Bulletin 16, 335-340.

A. Blackwell, A.J. Mordue (Luntz), B.S. Hansson, L.J. Wadhams and J.A. Pickett (1993) A behavioural and electrophysiological study of oviposition cues for Culex quinquefasciatus. Physiological Entomology 18, 343-348.

J.A. Pickett and C.M. Woodcock (1996) The role of mosquito olfaction in oviposition site location and in the avoidance of unsuitable hosts. In: Olfaction in Mosquito-Host Interactions. CIBA Foundation Symposium No. 200, 109-123. Editor G. Cardew. (John Wiley & Sons Ltd., Chichester).

L.E.G. Mboera, K.Y. Mdira, F.M. Salum, W. Takken and J.A. Pickett (1999) Influence of synthetic oviposition pheromone and volatiles from soakage pits and grass infusions upon oviposition site-selection of Culex mosquitoes in Tanzania. Journal of Chemical Ecology 25, 1855-1865.

L.E.G. Mboera, W. Takken, K.Y. Mdira, G.J. Chuwa and J.A. Pickett (2000) Oviposition and behavioral responses of Culex quinquefasciatus to skatole and synthetic oviposition pheromone in Tanzania. Journal of Chemical Ecology 26, 1193-1203.

L.E.G. Mboera, W. Takken, K.Y. Mdira and J.A. Pickett (2000) Sampling gravid Culex quinquefasciatus (Diptera: Culicidae) in Tanzania with traps baited with synthetic oviposition pheromone and grass infusions. Journal of Medical Entomology 37, 172-176.

T.O. Olagbemiro, M.A. Birkett, J.A. Pickett and A.J. Mordue (Luntz). (1999). Production of the mosquito oviposition pheromone, (5R, 6S)-6-acetoxy-5-hexadecanolide, from the seed oil of the Summer Cypress plant, Kochia scoparia (Chenopodiaceae). Journal of Agricultural and Food Chemistry, 47, 3411-3415.

T.O.Olagbemiro, M.A. Birkett, A.J. Mordue (Luntz) and J.A. Pickett (2004) Laboratory and field responses of the pathogen-vectoring mosquito, Culex quinquefasciatus, to plant-derived oviposition pheromone and the oviposition cue skatole. Journal of Chemical Ecology, 965-976.

J.G.C. Hamilton, G.W. Dawson and J.A. Pickett (1996) 3-Methyl-α-himachalene; proposed structure for the novel homosesquiterpene sex pheromone of Lutzomyia longipalpis (Diptera: Psychodidae) from Jacobina, Brazil. Journal of Chemical Ecology 22, 2331-2340.

J.G.C. Hamilton, G.W. Dawson and J.A. Pickett (1996) 9-Methylgermacrene-B; proposed structure for novel homosesquiterpene from the sex pheromone glands of Lutzomyia longipalpis (Diptera: Psychodidae) from Lapinha, Brazil. Journal of Chemical Ecology 22, 1477-1491.

J.G.C. Hamilton, A.M. Hooper, K. Mori, J.A. Pickett and S. Sano (1999) 3-Methyl-α-himachalene is confirmed, and the relative stereochemistry defined, by synthesis as the sex pheromone of the sandfly Lutzomyia longipalpis from Jacobina, Brazil. Chemical Communications, 355-356.

J.G.C. Hamilton, A.M. Hooper, H.C. Ibbotson, S. Kurosawa, K. Mori, S. Muto and J.A. Pickett (1999) 9-Methylgermacrene-B is confirmed as the sex pheromone of the sandfly Lutzomyia longipalpis from Lapinha, Brazil, and the absolute stereochemistry defined as S. Chemical Communications, 2335-2336.

A.M. Hooper, J-B. Farcet, N.P. Mulholland and J.A. Pickett (2006) Synthesis of 9-methylgermacrene B, racemate of the sex pheromone of Lutzomyia longipalpis (Lapinha), from the renewable resource, Geranium macrorrhizum essential oil. Green Chemistry 8, 513-515.

A. Ingvarsdottir, M.A. Birkett, I. Duce, W. Mordue, J.A. Pickett, L.J. Wadhams and A.J. Mordue (Luntz) (2002). Behavioural responses of the parasitic sea lice Lepeoptheirus salmonis to mating related semiochemicals. Journal of Chemical Ecology, 28, 10, 2107-2117.

Kilpinen, O., Steenberg, T., Jespersen, J.B., Cruz, M.D.S., Vega Robles, C., Birkett, M.A., Dewhirst, S. and Pickett, J. (2002). Advances in the development of alternative control methods against chicken mites. Proceedings Mange and myiasis in livestock annual meeting, 18-21 September 2002.

Cruz M.D.S, Vega Robles, M.C., Jespersen, J.B., Kilpinen, O., Birkett, M., Dewhirst, S. and Pickett, J. (2005). Scanning electron microscopy of foreleg tarsal sense organs of the poultry red mite, Dermanyssus gallinae (DeGeer) (Acari:Dermanyssidae) Micron, 36 (5): 415-421.

A.C. Skelton, M.A. Birkett, J.A. Pickett and M.M. Cameron (2007) Olfactory responses of medically and economically important mites (Acari: Epidermoptidae and Acaridae) to volatile chemicals. Journal of Medical Entomology 44, 367-371.

Figures

Figure 1A. Culex spp. oviposition pheromone (5R,6S-6-acetoxy-5-hexadecanolide)

Figure 1B. Human-specific acids. Mosquito repellents

Figure 1C. 6-Methyl-5-hepten-2-one. Horn fly repellent

Figure 1D. Sealice semiochemicals. Host and non-host kairomones

Figure 1E. Sandfly sex pheromones

Figure 2. Differential loads of horn flies, Haematobia irritans, on herds of Holstein-Friesian Cattle

Figure 3. Air entrainment to isolate semiochemicals from human beings The yellow fever mosquito, Aedes aegypti, mosquito Electroantennogram schematic