Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-23T05:16:18.928Z Has data issue: false hasContentIssue false
  • English
  • Français

Biting behaviour of Tabanidae on cattle in mountainous summer pastures, Pyrenees, France, and effects of weather variables

Published online by Cambridge University Press:  12 March 2014

F. Baldacchino ,
L. Puech ,
S. Manon ,
Lionel R. Hertzog  and
P. Jay-Robert
F. Baldacchino*
Affiliation:
UMR 5175, Centre d'Ecologie Fonctionnelle et Evolutive (CEFE), Université Paul-Valéry (UM3), 34199 Montpellier Cedex 5, France
L. Puech
Affiliation:
UMR 5175, Centre d'Ecologie Fonctionnelle et Evolutive (CEFE), Université Paul-Valéry (UM3), 34199 Montpellier Cedex 5, France
S. Manon
Affiliation:
UMR 5175, Centre d'Ecologie Fonctionnelle et Evolutive (CEFE), Université Paul-Valéry (UM3), 34199 Montpellier Cedex 5, France
Lionel R. Hertzog
Affiliation:
Center for Food and Life Science Weihenstephan, Technische Universität München, 85354 Freishing, Germany
P. Jay-Robert
Affiliation:
UMR 5175, Centre d'Ecologie Fonctionnelle et Evolutive (CEFE), Université Paul-Valéry (UM3), 34199 Montpellier Cedex 5, France
*
*Author for correspondence Phone: +33467142461 Fax: +33467142459 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

In France, during the summer, cattle in mountainous pastures can be highly exposed to tabanid bites. The persistent biting behaviour of tabanids not only causes disturbance, but is also responsible for transmitting diseases, such as bovine besnoitiosis. The purpose of this study was to better identify the level of tabanid annoyance on cattle by means of insect trapping and direct observation of cows. Tabanids were active during the entire daily observation period (10:00–16:00), except for Haematopota sp., which were less active in the morning. The tabanids collected in Nzi traps were generally representative of those that landed on cattle, except for Haematopota sp., as Nzi traps were not very effective for these species. The preferred feeding sites for most species appeared to be cow's legs or udder. Leg stamping was the defensive reaction most related to a tabanid alighting on a host. Generalized linear mixed models showed that the parameters associated with tabanid landings on hosts were related to weather and altitude, but not to landscape structure. Increased landings were mostly associated with the higher temperatures and lower wind speeds at midday, but some differences were observed between species. The results indicate that cattle-protection measures should be taken during the peak of tabanid abundance when climatic conditions favour intense biting activity. Nzi traps set close to livestock were very effective to catch tabanids and could help in reducing the annoyance caused by horse flies.

Keywords

Tabanidaebiting behaviourdefensive behaviourhorse fliesNzi trapweather
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 104 , Issue 4 , August 2014 , pp. 471 - 479
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alvarez-García, G., Frey, C.F., Mora, L.M. & Schares, G. (2013) A century of bovine besnoitiosis: an unknown disease re-emerging in Europe. Trends in Parasitology 29, 407–415. doi: 10.1016/j.pt.2013.06.002.CrossRefGoogle ScholarPubMed
Alverson, D.R. & Noblet, R. (1977) Activity of female Tabanidae (Diptera) in relation to selected meteorological factors in South Carolina. Journal of Medical Entomology 4, 197–200.CrossRefGoogle Scholar
Amano, K. (1985) Statistical analyses of the influence of meteorological factors on flight activity of female tabanids. Kontyû, Tokyo 53, 161–172.Google Scholar
Baldacchino, F., Cadier, J., Porciani, A., Buatois, B., Dormont, L. & Jay-Robert, P. (2013 a) Behavioural and electrophysiological responses of females of two species of tabanid to volatiles in urine of different mammals. Medical and Veterinary Entomology 27, 77–85.Google Scholar
Baldacchino, F., Gardes, L., De Stordeur, E., Jay-Robert, P. & Garros, C. (2013 b) Blood-feeding patterns of horse flies in the French Pyrenees. Veterinary Parasitology 199, 283–288.Google Scholar
Baldacchino, F., Manon, S., Puech, L., Buatois, B., Dormont, L. & Jay-Robert, P. (2013 c) Olfactory and behavioural responses of tabanids to octenol, phenols and aged horse urine. Medical and Veterinary Entomology, DOI: 10.1111/mve.12038.Google Scholar
Baldacchino, F., Porciani, A., Bernard, C. & Jay-Robert, P. (2013 d) Spatial and temporal distribution of Tabanidae in the Pyrenees Mountains: influence of altitude and landscape structure. Bulletin of Entomological Research 104, 1–11.CrossRefGoogle ScholarPubMed
Barros, A.T.M. & Foil, L.D. (2007) The influence of distance on movement of tabanids (Diptera: Tabanidae) between horses. Veterinary Parasitology 144, 380–384.Google Scholar
Bates, D., Maechler, M. & Bolker, B. (2012) lme4: Linear mixed-effects models using S4 classes. Available online at http://cran.r-project.org/web/packages/lme4/index.html Google Scholar
Baylis, M. (1996) Effect of defensive behaviour by cattle on the feeding success and nutritional state of the tsetse fly, Glossina pallidipes (Diptera: Glossinidae). Bulletin of Entomological Research 86, 329–336.CrossRefGoogle Scholar
Bell, J.R., Aralimarad, P., Lim, K.-S. & Chapman, J.W. (2013) Predicting insect migration density and speed in the daytime convective boundary layer. Plos ONE 8, e54202. doi: 10.1371/journal.pone.0054202.Google Scholar
Bigalke, R.D. (1968) New concepts on the epidemiological features of bovine besnoitiosis as determined by laboratory and field investigations. The Onderstepoort Journal of Veterinary Research 35, 3–137.Google ScholarPubMed
Blahó, M., Egri, A., Barta, A., Antoni, G., Kriska, G. & Horváth, G. (2012) How can horseflies be captured by solar panels? A new concept of tabanid traps using light polarization and electricity produced by photovoltaics. Veterinary Parasitology 189, 353–365.Google Scholar
Bolker, B.M., Brooks, M.E., Clark, C.J., Geange, S.W., Poulsen, J.R., Stevens, M.H.H. & White, J.-S.S. (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology & Evolution 24, 127–135.CrossRefGoogle ScholarPubMed
Burnett, A.M. & Hays, K.L. (1974) Some influences of meteorological factors on flight activity of female horse flies (Diptera: Tabanidae). Environmental Entomology 3, 515–521.CrossRefGoogle Scholar
Chvála, M. (1979) Daily activity of Tabanidae in the Caucasus. Angewandte Parasitologie 20, 38–45.Google Scholar
Chvála, M., Lyneborg, L. & Moucha, J. (1972) The Horse Flies of Europe (Diptera, Tabanidae). Copenhagen, Entomological Society of Copenhagen.CrossRefGoogle Scholar
Crawley, M.J. (2007) The R Book. West Sussex, John Wiley & Sons Ltd.Google Scholar
Dale, W.E. & Axtell, R.C. (1975) Flight of the salt marsh Tabanidae (Diptera), Tabanus nigrovittatus, Chrysops atlanticus and C. fuliginosus: correlation with temperature, light, moisture and wind velocity. Journal of Medical Entomology 12, 551–557.Google Scholar
Desquesnes, M., Biteau-Coroller, F., Bouyer, J., Dia, M.L. & Foil, L. (2009) Development of a mathematical model for mechanical transmission of trypanosomes and other pathogens of cattle transmitted by tabanids. International Journal for Parasitology 39, 333–346.CrossRefGoogle ScholarPubMed
Egri, A., Blahó, M., Szaz, D., Barta, A., Kriska, G., Antoni, G. & Horváth, G. (2013 a) A new tabanid trap applying a modified concept of the old flypaper: linearly polarising sticky black surfaces as an effective tool to catch polarotactic horseflies. International Journal for Parasitology 43, 555–563.Google Scholar
Egri, A., Blahó, M., Szaz, D., Kriska, G., Majer, J., Herczeg, T., Gyurkovszky, M., Farkas, R. & Horváth, G. (2013 b) A horizontally polarizing liquid trap enhances the tabanid-capturing efficiency of the classic canopy trap. Bulletin of Entomological Research 103, 665–674.Google Scholar
Foil, L. & Foil, C. (1988) Dipteran parasites of horses. Equine Practice 10, 21–38.Google Scholar
Foil, L.D. & Hogsette, J.A. (1994) Biology and control of tabanids, stable flies and horn flies. Revue Scientifique et Technique 13, 1125–1158.Google Scholar
Foil, L.D. & Issel, C.J. (1991) Transmission of retroviruses by arthropods. Annual Reviews of Entomology 36, 355–381.CrossRefGoogle ScholarPubMed
Foil, L.D., Meek, C.L., Adams, W.V. & Issel, C.J. (1983). Mechanical transmission of equine infectious anemia virus by deer flies (Chrysops flavidus) and stable flies (Stomoxys calcitrans). American Journal Veterinary Research 44, 155–156.Google Scholar
Gibson, G. & Torr, S.J. (1999) Visual and olfactory responses of haematophagous Diptera to host stimuli. Medical and Veterinary Entomology 13, 2–23.CrossRefGoogle ScholarPubMed
Gilles, J., David, J.F., Duvallet, G., De La Rocque, S. & Tillard, E. (2007) Efficiency of traps for Stomoxys calcitrans and Stomoxys niger niger on Reunion Island. Medical and Veterinary Entomology 21, 65–69.CrossRefGoogle ScholarPubMed
Hackenberger, B.K., Jarić, D. & Krčmar, S. (2009) Distribution of tabanids (Diptera: Tabanidae) along a two-sided altitudinal transect. Environmental Entomology 38, 1600–1607.Google Scholar
Hans, A., Poncon, N. & Zientara, S. (2012) Epidemiology of equine infectious anemia in France and in Europe from 1994 to 2011. Bulletin De l'Académie Vétérinaire De France 165, 27–34.Google Scholar
Hart, B.L. (1992) Behavioral adaptations to parasites: an ecological approach. Journal of Parasitology 78, 256–265.Google Scholar
Hollander, A.L. & Wright, R.E. (1980) Impact of tabanids (Diptera: Tabanidae) on cattle: blood meal size and preferred feeding sites. Journal of Economic Entomology 73, 431–433.Google Scholar
Horváth, G., Majer, J., Horváth, L., Szivak, I. & Kriska, G. (2008) Ventral polarization vision in tabanids: horseflies and deerflies (Diptera : Tabanidae) are attracted to horizontally polarized light. Naturwissenschaften 95, 1093–1100.Google Scholar
Horváth, G., Blahó, M., Kriska, G., Hegedüs, R., Gerics, B., Farkas, R. & Akesson, S. (2010) An unexpected advantage of whiteness in horses: the most horsefly-proof horse has a depolarizing white coat. Proceedings of the Royal Society B-Biological Sciences 277, 1643–1650.Google Scholar
Hribar, L.J., Leprince, D.J. & Foil, L.D. (1992) Feeding sites of some Louisiana Tabanidae (Diptera) on fenvalerate-treated and control cattle. Journal of Economic Entomology 85, 2279–2285.Google Scholar
Hughes, R.D., Duncan, P. & Dawson, J. (1981) Interactions between Camargue Horses and Horseflies (Diptera: Tabanidae). Bulletin of Entomological Research 71, 227–242.Google Scholar
Jacquiet, P., Lienard, E. & Franc, M. (2010). Bovine besnoitiosis: epidemiological and clinical aspects. Veterinary Parasitology 174, 30–36.Google Scholar
Krčmar, S. & Marić, S. (2006) Analysis of the feeding sites for some horse flies (Diptera, Tabanidae) on a human in Croatia. Collegium Antropologicum 30, 901–904.Google Scholar
Lewis, D.J. & Leprince, D.J. (1981) Horse flies and Deer flies (Diptear: Tabanidae) feeding on cattle in southwestern Quebec. Canadian Entomologist 113, 883–886.CrossRefGoogle Scholar
Mihok, S. (2002) The development of a multipurpose trap (the Nzi) for tsetse and other biting flies. Bulletin of Entomological Research 92, 385–403.Google Scholar
Mihok, S. & Lange, K. (2012) Synergism between ammonia and phenols for Hybomitra tabanids in northern and temperate Canada. Medical and Veterinary Entomology 26, 282–290.Google Scholar
Mihok, S. & Mulye, H. (2010) Responses of tabanids to Nzi traps baited with octenol, cow urine and phenols in Canada. Medical and Veterinary Entomology 24, 266–272.Google ScholarPubMed
Mihok, S., Carlson, D.A., Krafsur, E.S. & Foil, L.D. (2006) Performance of the Nzi and other traps for biting flies in North America. Bulletin of Entomological Research 96, 387–397.Google Scholar
Mohamed-Ahmed, M.M. & Mihok, S. (2009) Alighting of Tabanidae and muscids on natural and simulated hosts in the Sudan. Bulletin of Entomological Research 99, 561–571.Google Scholar
Mooring, M.S., Blumstein, D.T., Reisig, D.D., Osborne, E.R. & Niemeyer, J.M. (2007) Insect-repelling behaviour in bovids: role of mass, tail length, and group size. Biological Journal of the Linnean Society 91, 383–392.Google Scholar
Mullen, G.R. & Durden, L.A. (2002) Medical and Veterinary Entomology. Amsterdam, Academic Press.Google Scholar
Mullens, B.A. & Gerhardt, R.R. (1979) Feeding-behavior of some Tennessee Tabanidae. Environmental Entomology 8, 1047–1051.Google Scholar
Mullens, B.A., Lii, K.S., Mao, Y., Meyer, J.A., Peterson, N.G. & Szijj, C.E. (2006) Behavioural responses of dairy cattle to the stable fly, Stomoxys calcitrans, in an open field environment. Medical and Veterinary Entomology 20, 122–137.Google Scholar
Muzari, M.O., Skerratt, L.F., Jones, R.E. & Duran, T.L. (2010) Alighting and feeding behaviour of tabanid flies on horses, kangaroos and pigs. Veterinary Parasitol 170, 104–111.Google Scholar
Perich, M.J., Wright, R.E. & Lusby, K.S. (1986) Impact of horse flies (Diptera: Tabanidae) on beef-cattle. Journal of Economic Entomology 79, 128–131.Google Scholar
Phelps, R.J. & Holloway, M.T.P. (1990) Alighting sites of female Tabanidae (Diptera) at Rekomitjie, Zimbabwe. Medical and Veterinary Entomology 4, 349–356.Google Scholar
Ralley, W.E., Galloway, T.D. & Crow, G.H. (1993) Individual and group-behavior of pastured cattle in response to attack by biting flies. Canadian Journal of Zoology-Revue Canadienne De Zoologie 71, 725–734.CrossRefGoogle Scholar
Raymond, H.L. & Rousseau, F. (1987) Abundance of horse flies (Diptera, Tabanidae) and reactions of cattle in a traditionnal farm of French-Guiana. Acta Oecologica-Oecologia Applicata 8, 125–134.Google Scholar
R Development Core Team (2013) R: A Language and Environment for Statistical Computing. Vienna, Austria, R Foundation for Statistical Computing. Available online at http://www.r-project.org/ Google Scholar
Sheppard, C. & Wilson, B.H. (1977) Relationship of horse fly host seeking activity to edge of wooded areas in southern Louisiana. Environmental Entomology 6, 781–782.CrossRefGoogle Scholar
Thomas, G.D., Berry, I.L., Berkebile, D.R. & Skoda, S.R. (1989) Comparisons of three sampling methods for estimating adult stable fly (Diptera: Muscidae) populations. Environmental Entomology 18, 513–520.Google Scholar
Torr, S.J. & Mangwiro, T.N.C. (2000) Interactions between cattle and biting flies: effects on the feeding rate of tsetse. Medical and Veterinary Entomology 14, 400–409.Google Scholar
Van Hennekeler, K., Jones, R.E., Skerratt, L.F., Muzari, M.O. & Fitzpatrick, L.A. (2011) Meteorological effects on the daily activity patterns of tabanid biting flies in northern Queensland, Australia. Medical and Veterinary Entomology 25, 17–24.Google Scholar
Warnes, M.L. & Finlayson, L.H. (1987) Effect of host behavior on host preference in Stomoxys calcitrans . Medical and Veterinary Entomology 1, 53–57.Google Scholar
Wilson, B.H. (1968) Reduction of Tabanid populations on cattle with sticky traps baited with dry ice. Journal of Economic Entomology 61, 827–829.Google Scholar
Zardi, D. & Whiteman, D. (2012) Diurnal mountain wind systems. pp. 35–119 in Chow, F. et al. (Eds) Mountain Weather Research and Forecasting. Berlin, Springer.Google Scholar
Zuur, A., Ieno, E.N., Walker, N., Saveliev, A.A. & Smith, G.M. (2009) Mixed Effects Models and Extensions in Ecology with R. New-York, Springer Science+Buisness Media.Google Scholar
Supplementary material: Image

Baldacchino Supplementary Material

Figure

Download Baldacchino Supplementary Material(Image)
Image 1.2 MB
Supplementary material: File

Baldacchino Supplementary Material

Supplementary Material

Download Baldacchino Supplementary Material(File)
File 52.2 KB
Supplementary material: File

Baldacchino Supplementary Material

Figure Caption

Download Baldacchino Supplementary Material(File)
File 26.1 KB