Water vapour and heat combine to elicit biting and biting persistence in tsetse

Particle and Fibre Toxicology

Patrick M Guerin¹  Michèle Vlimant¹  Steve Béguin¹  Charles JF Chappuis¹ 

[1] Institute of Biology, Laboratory of Animal Physiology, University of Neuchâtel, Rue Emile-Argand 11, 2000, Neuchâtel, Switzerland

关键词: Dry cell;    Thermoreception;    Hygroreception;    Blood-feeding;    Biting fly;    Biting behaviour;    Glossina pallidipes;    Tsetse;   

Others  :  824875
DOI  :  10.1186/1756-3305-6-240

 received in 2013-05-14, accepted in 2013-08-09,  发布年份 2013

【 摘 要 】

Background

Tsetse flies are obligatory blood feeders, accessing capillaries by piercing the skin of their hosts with the haustellum to suck blood. However, this behaviour presents a considerable risk as landing flies are exposed to predators as well as the host’s own defense reactions such as tail flicking. Achieving a successful blood meal within the shortest time span is therefore at a premium in tsetse, so feeding until replete normally lasts less than a minute. Biting in blood sucking insects is a multi-sensory response involving a range of physical and chemical stimuli. Here we investigated the role of heat and humidity emitted from host skin on the biting responses of Glossina pallidipes, which to our knowledge has not been fully studied in tsetse before.

Methods

The onset and duration of the biting response of G. pallidipes was recorded by filming movements of its haustellum in response to rapid increases in temperature and/or relative humidity (RH) following exposure of the fly to two airflows. The electrophysiological responses of hygroreceptor cells in wall-pore sensilla on the palps of G. pallidipes to drops in RH were recorded using tungsten electrodes and the ultra-structure of these sensory cells was studied by scanning and transmission electron microscopy.

Results

Both latency and proportion of tsetse biting are closely correlated to RH when accompanied by an increase of 13.1°C above ambient temperature but not for an increase of just 0.2°C. Biting persistence, as measured by the number of bites and the time spent biting, also increases with increasing RH accompanied by a 13.1°C increase in air temperature. Neurones in wall-pore sensilla on the palps respond to shifts in RH.

Conclusions

Our results show that temperature acts synergistically with humidity to increase the rapidity and frequency of the biting response in tsetse above the levels induced by increasing temperature or humidity separately. Palp sensilla housing hygroreceptor cells, described here for the first time in tsetse, are involved in the perception of differences in RH.

【 授权许可】

   
2013 Chappuis et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Gibson G, Torr S: Visual and olfactory responses of haematophagous diptera to host stimuli. Med Vet Entomol 1999, 13:2-23.
• [2]Randolph SE, Williams BG, Rogers DJ, Connor H: Modelling the effect of feeding related mortality on the feeding strategy of tsetse (Diptera: Glossinidae). Med Vet Entomol 1992, 6:231-240.
• [3]Carey JR: Insect biodemography. Annu Rev Entomol 2001, 46:79-110.
• [4]Snow W, Tarimo S: Observations on age-grouping the tsetse fly, Glossina pallidipes, by wing-fray and ovarian dissection, on the south Kenya coast. Ann Trop Med Parasitol 1985, 79:457.
• [5]Randolph SE, Rogers DJ, Kiilu J: The feeding behavior, activity and trapability of wild female Glossina pallidipes in relation to their pregnancy cycle. Med Vet Entomol 1991, 5:335-350.
• [6]Turner D: The population ecology of Glossina pallidipes Austen (Diptera: Glossinidae) in the Lambwe Valley, Kenya. I. Feeding behaviour and activity patterns. Bull Entomol Res 1987, 77:317-333.
• [7]Dethier VG: Notes on the biting response of tsetse flies. Am J Trop Med Hyg 1954, 3:160-171.
• [8]Kröber T, Guerin PM: An in vitro feeding assay to test acaricides for control of hard ticks. Pest Manag Sci 2007, 63:17-22.
• [9]Fresquet N, Lazzari CR: Response to heat in Rhodnius prolixus: the role of the thermal background. J Insect Physiol 2011, 57:1446-1449.
• [10]Aboul-Nasr A, Erakey M: On the behaviour and sensory physiology of the bedbug. I-Temperature reactions (Hemiptera: Cimicidae). Bull Soc Entomol Egypte 1967, 51:43-54.
• [11]Moskalyk L, Friend W: Feeding behaviour of female Aedes aegypti: effects of diet temperature, bicarbonate and feeding technique on the response to ATP. Physiol Entomol 1994, 19:223-229.
• [12]Lall SB: Phagostimulants of haematophagous tabanids (Diptera). Entomol Exp Appl 1969, 12:325-336.
• [13]Sutcliffe J, McIver SB: Artificial feeding of simuliids (Simulium venustum): factors associated with probing and gorging. Cell Mol Life Sci 1975, 31:694-695.
• [14]Van Naters WMV, Den Otter CJ, Cuisance D: The interaction of taste and heat on the biting response of the tsetse fly Glossina fuscipes fuscipes. Physiol Entomol 1998, 23:285-288.
• [15]Gatehouse A: Synergistic effect of two stimulants to induce probing in Stomoxys calcitrans (L.). Nature (Lond) 1967, 216:794-795.
• [16]Gatehouse A: Interactions between stimuli in the induction of probing by Stomoxys calcitrans. J Insect Physiol 1970, 16:991-1000.
• [17]Gatehouse A: The probing response of Stomoxys calcitrans to certain physical and olfactory stimuli. J Insect Physiol 1970, 16:61-74.
• [18]Evans WG, Gooding RH: Turbulent plumes of heat, moist heat, and carbon dioxide elicit upwind anemotaxis in tsetse flies Glossina morsitans morsitans Westwood (Diptera : Glossinidae). Can J Zool 2002, 80:1149-1155.
• [19]Eiras AE, Jepson P: Responses of female Aedes aegypti (Diptera: Culicidae) to host odours and convection currents using an olfactometer bioassay. Bull Entomol Res 1994, 84:207-212.
• [20]McLean J: The partition of insensible losses of body weight and heat from cattle under various climatic conditions. J Physiol 1963, 167:427-447.
• [21]Sokolov VE: Mammal skin. Berkeley, Los-Angeles, London: Univ of California Press; 1982.
• [22]Taneja J, Guerin PM: Oriented responses of the triatomine bugs Rhodnius prolixus and Triatoma infestans to vertebrate odours on a servosphere. J Comp Physiol A Sens Neural Behav Physiol 1995, 176:455-464.
• [23]Buck AL: New equations for computing vapor pressure and enhancement factor. J Appl Meteorol 1981, 20:1527-1532.
• [24]Kinovea. http://www.kinovea.org/ webcite
• [25]R: A language and environment for statistical computing. http://www.cran.r-project.org/ webcite
• [26]Kessler S, Vlimant M, Guerin PM: The sugar meal of the African malaria mosquito Anopheles gambiae and how deterrent compounds interfere with it: a behavioural and neurophysiological study. J Exp Biol 2013, 216:1292-1306.
• [27]Taneja J, Guerin PM: Ammonia attracts the haematophagous bug Triatoma infestans: Behavioural and neurophysiological data on nymphs. J Comp Physiol A Sens Neural Behav Physiol 1997, 181:21-34.
• [28]Moloo S, Gettinby G, Olubayo R, Kabata J, Okumu I: A comparison of African buffalo, N’Dama and Boran cattle as reservoirs of Trypanosoma vivax for different Glossina species. Parasitology 1993, 106:277-282.
• [29]Moloo SK, Kutuza SB, Boreham PFL: Studies on Glossina pallidipes, Glossina fuscipes fuscipes And Glossina brevipalpis in terms of the epidemiology and epizootiology of trypanosomiases in southeastern Uganda. Ann Trop Med Parasitol 1980, 74:219-237.
• [30]Allen T, Bennett J, Donegan SM, Hutchinson J: Moisture, its accumulation and site of evaporation in the coats of sweating cattle. J agric Sci 1970, 74:247-258.
• [31]Ingram D, McLean J, Whittow G: The effect of heating the hypothalamus and the skin on the rate of moisture vaporization from the skin of the ox (Bos taurus). J Physiol 1963, 169:394-403.
• [32]Ferguson K, Dowling D: The function of cattle sweat glands. Crop and Pasture Science 1955, 6:640-644.
• [33]Khan A, Maibach H: Study of the probing response of aedes aegypti. 1 4. Effect of Dry and moist heat on probing. J Econ Entomol 1971, 64:442-443.
• [34]Brady J: Changes in the probing responsiveness of starving tsetse flies (Glossina morsitans Westw.) (Diptera, Glossinidae). Bull Entomol Res 1973, 63:247-255.
• [35]Langley P, Maly H: Membrane feeding technique for tsetse flies (Glossina spp.). Nature (Lond) 1969, 221:855-856.
• [36]Terblanche JS, Chown SL: The effects of temperature, body mass and feeding on metabolic rate in the tsetse fly Glossina morsitans centralis. Physiol Entomol 2007, 32:175-180.
• [37]Von Arx M, Goyret J, Davidowitz G, Raguso RA: Floral humidity as a reliable sensory cue for profitability assessment by nectar-foraging hawkmoths. Proc Natl Acad Sci USA 2012, 109:9471-9476.
• [38]Bursell E: The effect of humidity on the activity of tsetse flies. J Exp Biol 1957, 34:42-51.
• [39]Kleynhans E, Terblanche JS: Complex interactions between temperature and relative humidity on water balance of adult tsetse (Glossinidae, Diptera): implications for climate change. Front Physiol 2011, 2:1-10.
• [40]Chown SL, Sørensen JG, Terblanche JS: Water loss in insects: an environmental change perspective. J Insect Physiol 2011, 57:1070-1084.
• [41]Kessler S, Guerin PM: Responses of Anopheles gambiae, Anopheles stephensi, Aedes aegypti, and Culex pipiens mosquitoes (Diptera: Culicidae) to cool and humid refugium conditions. J Vector Ecol 2008, 33:145-149.
• [42]Shanbhag S, Müller B, Steinbrecht R: Atlas of olfactory organs of Drosophila melanogaster: 1. Types, external organization, innervation and distribution of olfactory sensilla. Int J Insect Morphol Embryol 1999, 28:377-397.
• [43]Lewis CT: Observations on the palps of tsetse flies. Trans R Soc Trop Med Hyg 1972, 66:318-319.
• [44]Altner H, Loftus R: Ultrastructure and function of insect thermo-and hygroreceptors. Annu Rev Entomol 1985, 30:273-295.
• [45]Tichy H, Kallina W: Insect hygroreceptor responses to continuous changes in humidity and air pressure. J Neurophysiol 2010, 103:3274-3286.