A 3D Analysis of Flight Behavior of Anopheles gambiae sensu stricto Malaria Mosquitoes in Response to Human Odor and Heat

Female mosquitoes use odor and heat as cues to navigate to a suitable landing site on their blood host. The way these cues affect flight behavior and modulate anemotactic responses, however, is poorly understood. We studied in-flight behavioral responses of females of the nocturnal malaria mosquito Anopheles gambiae sensu stricto to human odor and heat. Flight-path characteristics in a wind tunnel (flow 20 cm/s) were quantified in three dimensions. With wind as the only stimulus (control), short and close to straight upwind flights were recorded. With heat alone, flights were similarly short and direct. The presence of human odor, in contrast, caused prolonged and highly convoluted flight patterns. The combination of odor+heat resulted in longer flights with more landings on the source than to either cue alone. Flight speed was greatest (mean groundspeed 27.2 cm/s) for odor+heat. Odor alone resulted in decreased flight speed when mosquitoes arrived within 30 cm of the source whereas mosquitoes exposed to odor+heat maintained a high flight speed while flying in the odor plume, until they arrived within 15 cm of the source. Human odor evoked an increase in crosswind flights with an additive effect of heat at close range (<15 cm) to the source. This was found for both horizontal and vertical flight components. However, mosquitoes nevertheless made upwind progress when flying in the odor+heat generated plume, suggesting that mosquitoes scan their environment intensively while they progress upwind towards their host. These observations may help to improve the efficacy of trapping systems for malaria mosquitoes by (1) optimizing the site of odor release relative to trap entry and (2) adding a heat source which enhances a landing response.

[1]  S. Krčmar,et al.  Response of Tabanidae (Diptera) to natural and synthetic olfactory attractants. , 2005, Journal of vector ecology : journal of the Society for Vector Ecology.

[2]  Barbara Webb,et al.  A model of visual–olfactory integration for odour localisation in free-flying fruit flies , 2010, Journal of Experimental Biology.

[3]  W. Mordue,et al.  Field studies on efficacy of host odour baits for the biting midge Culicoides impunctatus in Scotland , 2001, Medical and veterinary entomology.

[4]  W. Takken,et al.  Effectiveness of Synthetic Versus Natural Human Volatiles as Attractants for Anopheles gambiae (Diptera: Culicidae) Sensu Stricto , 2010, Journal of medical entomology.

[5]  M. J. Packer,et al.  Orientation of tsetse flies to wind, within and outside host odour plumes in the field , 1991 .

[6]  G. Gibson,et al.  A behavioural test of the sensitivity of a nocturnal mosquito, Anopheles gambiae, to dim white, red and infra‐red light , 1995 .

[7]  J. Laarman The host-seeking behaviour of anopheline mosquitoes. , 1958, Tropical and geographical medicine.

[8]  M. Dacke,et al.  Flight behaviour of the hawkmoth Manduca sexta towards unimodal and multimodal targets , 2010, Journal of Experimental Biology.

[9]  G. Gibson,et al.  Flight behaviour of tsetse flies in host odour plumes: the initial response to leaving or entering odour , 1988 .

[10]  W. Takken,et al.  Olfaction in vector-host interactions , 2010 .

[11]  Robert C. Wolpert,et al.  A Review of the , 1985 .

[12]  M. Gillies.,et al.  The range of attraction of single baits for some West African mosquitoes. , 1970, Bulletin of entomological research.

[13]  W. Takken,et al.  Trapping of the malaria vector Anopheles gambiae with odour-baited MM-X traps in semi-field conditions in western Kenya , 2006, Malaria Journal.

[14]  D. G. Peterson,et al.  Studies of the Responses of the Female Aëdes Mosquito. Part III. The Response of Aëdes aegypti (L.) to a warm Body and its Radiation. , 1951 .

[15]  G. Gibson,et al.  Visual and olfactory responses of haematophagous Diptera to host stimuli , 1999, Medical and veterinary entomology.

[16]  R. Cardé,et al.  Influence of plume structure and pheromone concentration on upwind flight of Cadra cautella males , 1995 .

[17]  R T Cardé,et al.  Orientation of Culex mosquitoes to carbon dioxide‐baited traps: flight manoeuvres and trapping efficiency , 2006, Medical and veterinary entomology.

[18]  W. Takken,et al.  Anopheles gambiae TRPA1 is a heat‐activated channel expressed in thermosensitive sensilla of female antennae , 2009, The European journal of neuroscience.

[19]  W. Takken,et al.  Odor-mediated behavior of Afrotropical malaria mosquitoes. , 1999, Annual Review of Entomology.

[20]  W. Takken,et al.  A Novel Synthetic Odorant Blend for Trapping of Malaria and Other African Mosquito Species , 2012, Journal of Chemical Ecology.

[21]  F. E. Kellogg,et al.  The Guidance of Flying Insects. V. Mosquito Attraction , 1962, Canadian Entomologist.

[22]  Willem Takken,et al.  Host finding by female mosquitoes: mechanisms of orientation to host odours and other cues. , 2010 .

[23]  W. Takken,et al.  Attractiveness of MM-X Traps Baited with Human or Synthetic Odor to Mosquitoes (Diptera: Culicidae) in The Gambia , 2007, Journal of medical entomology.

[24]  M. Dickinson,et al.  Free-flight responses of Drosophila melanogaster to attractive odors , 2006, Journal of Experimental Biology.

[25]  W. Mukabana,et al.  Attraction of Anopheles gambiae to odour baits augmented with heat and moisture , 2010, Malaria Journal.

[26]  F. Howlett The Influence of Temperature upon the Biting of Mosquitoes , 1910, Parasitology.

[27]  Willem Takken,et al.  The Role of Olfaction in Host-Seeking of Mosquitoes: A Review , 1991 .

[28]  T. Baker,et al.  Reiterative responses to single strands of odor promote sustained upwind flight and odor source location by moths. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[29]  William J. Bell,et al.  Chemical Ecology of Insects , 1985, Springer US.

[30]  R. Cardé,et al.  Fine-scale structure of pheromone plumes modulates upwind orientation of flying moths , 1994, Nature.

[31]  W. Takken,et al.  Odor-mediated flight behavior ofAnopheles gambiae gilesSensu Stricto andAn. stephensi liston in response to CO2, acetone, and 1-octen-3-ol (Diptera: Culicidae) , 1997, Journal of Insect Behavior.

[32]  E. S. Lacey,et al.  Location of and landing on a source of human body odour by female Culex quinquefasciatus in still and moving air , 2012, Physiological entomology.

[33]  R T Cardé,et al.  Activation, orientation and landing of female Culex quinquefasciatus in response to carbon dioxide and odour from human feet: 3‐D flight analysis in a wind tunnel , 2011, Medical and veterinary entomology.

[34]  M. Geier,et al.  Carbon dioxide instantly sensitizes female yellow fever mosquitoes to human skin odours , 2005, Journal of Experimental Biology.

[35]  M. Gillies.,et al.  The Role of Carbon Dioxide in Host-Finding by Mosquitoes (Diptera: Culicidae): A Review , 1980 .

[36]  J. Visser,et al.  GENERAL GREEN LEAF VOLATILES IN THE OLFACTORY ORIENTATION OF THE COLORADO BEETLE, LEPTINOTARSA DECEMLINEATA , 1978 .

[37]  W. J. Bell,et al.  Chemical Ecology of Insects 2 , 1995, Springer US.

[38]  M. Copland,et al.  Human sweat and 2‐oxopentanoic acid elicit a landing response from Anopheles gambiae , 2000, Medical and veterinary entomology.

[39]  R. Cardé,et al.  Navigational Strategies Used by Insects to Find Distant, Wind-Borne Sources of Odor , 2008, Journal of Chemical Ecology.

[40]  W. Takken,et al.  Track 3D: Visualization and flight track analysis of Anopheles gambiae s.s. mosquitoes , 2008 .

[41]  B. Webster The role of olfaction in aphid host location , 2012 .

[42]  A. R. Jutsum,et al.  Insect pheromones in plant protection. , 1989 .

[43]  Ring T. Cardé,et al.  Moment-to-moment flight manoeuvres of the female yellow fever mosquito (Aedes aegypti L.) in response to plumes of carbon dioxide and human skin odour , 2011, Journal of Experimental Biology.

[44]  W. Takken,et al.  Composition of Human Skin Microbiota Affects Attractiveness to Malaria Mosquitoes , 2011, PloS one.

[45]  James M. Hyman,et al.  A Spatial Model of Mosquito Host-Seeking Behavior , 2012, PLoS Comput. Biol..

[46]  J. Halket,et al.  Landing responses of Anopheles gambiae elicited by oxocarboxylic acids , 2002, Medical and veterinary entomology.

[47]  Effect of the fine‐scale structure of pheromone plumes: pulse frequency modulates activation and upwind flight of almond moth males , 1995 .