Skip to main content

Advertisement

SpringerLink
Log in

Monitoring bluetongue virus vectors in Andalusia (SW Europe): Culicoides species composition and factors affecting capture rates of the biting midge Culicoides imicola

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

In this work, we summarize the results of captures of Culicoides species in Andalusia (S Spain) during 2007–2008. Four out of the 15 midge species—Culicoides imicola, Culicoides obsoletus complex, Culicoides pulicaris complex, and Culicoides nubeculosus—accounted for 80.7 % of captures (n = 68,190). Captures were seasonal and mostly occurred in May–November. The overall number of Culicoides specimens captured and the mean number of caught per trap were higher in 2007. We used an information-theoretic approach to analyze whether environmental factors (e.g., weather, altitude above the sea level, distance of the trap from the ground, distance to animals, and land use) affected C. imicola capture probability and success. Mean temperature and rainfall (both integrated into the Gaussen index), distance of traps to host animals, and trap height above the ground were the main factors explaining variance in capture rates in the Bluetongue Entomologic Surveillance Andalusian Program (BESAP). However, all of these patterns strongly varied among traps. As previously remarked by other authors, standardized capture methods and protocols for trap use are needed to ensure that results obtained in different geographical areas and/or periods are comparable.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Acevedo P, Ruiz-Fons F, Estrada R, Márquez AL, Miranda MA, Gortázar C, Lucientes J (2010) A broad assessment of factors determining Culicoides imicola abundance: modelling the present and forecasting its future in climate change scenarios. PLoS One 5:e14236

    Article  PubMed  CAS  Google Scholar 

  • Ander M, Meiswinkel R, Chirico J (2012) Seasonal dynamics of biting midges (Diptera: Ceratopogonidae: Culicoides), the potential vectors of bluetongue, in Sweden. Vet Parasitol 184:59–67

    Article  PubMed  CAS  Google Scholar 

  • Anderson DR, Burnham KP, White GA (2001) Kullback–Leibler information in resolving natural resource conflicts when definitive data exist. Wildl Soc Bull 29:1260–1270

    Google Scholar 

  • Bagnouls F, Gaussen H (1953) Saison sèche et indice xérothermique. Bull Soc Hist Nat Toulouse 88:193–240

    Google Scholar 

  • Balczun C, Vorsprach B, Meiser CK, Schaub GA (2009) Changes of the abundance of Culicoides obsoletus s.s. and Culicoides scoticus in Southwest Germany identified by a PCR-based differentiation. Parasitol Res 105:345–349

    Article  PubMed  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information–theoretic approach. Springer-Verlag, New York

    Google Scholar 

  • Calvete C, Estrada R, Miranda MA, Del Río R, Borrás D, Beldron FJ, Martínez A, Calvo AJ, Lucientes J (2010) Protection of livestock against bluetongue virus vector Culicoides imicola using insecticide-treated netting in open areas. Med Vet Entomol 24:169–175

    Article  PubMed  CAS  Google 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 153:71–74

    Article  PubMed  CAS  Google Scholar 

  • Carpenter S, Szmaragd C, Barber J, Labuschagne K, Gubbins S, Mellor P (2008) An assessment of Culicoides surveillance techniques in northern Europe: have we underestimated a potential bluetongue virus vector? J Appl Ecol 45:1237–1245

    Google Scholar 

  • Carpenter S, Wilson A, Mellor PS (2009) Culicoides and the emergence of bluetongue virus in northern Europe. Trends Microbiol 17:172–178

    Article  PubMed  CAS  Google Scholar 

  • Clausen PH, Stephan A, Bartsch S, Jandowsky A, Hoffmann-Köhler P, Schein E, Mehlitz D, Bauer B (2009) Seasonal dynamics of biting midges (Diptera: Ceratopogonidae, Culicoides spp.) on dairy farms of Central Germany during the 2007/2008 epidemic of bluetongue. Parasitol Res 105:381–386

    Article  PubMed  Google Scholar 

  • Conraths FJ, Gethmann JM, Staubach C, Mettenleiter TC, Beer M, Hoffmann B (2009) Epidemiology of bluetongue virus serotype 8, Germany. Emerg Infect Dis 15:433–435

    Article  PubMed  Google Scholar 

  • Consejería de Agricultura y Pesca, Junta de Andalucía (2012) Censo y producciones ganaderas. Available at: http://www.juntadeandalucia.es/agriculturaypesca/ Accessed on 7 February 2012

  • Conte A, Goffredo M, Ippoliti C, Meiswinkel R (2007) Influence of biotic and abiotic factors on the distribution and abundance of Culicoides imicola and the Obsoletus Complex in Italy. Vet Parasitol 150:333–334

    Article  PubMed  CAS  Google Scholar 

  • Del Río R, Monerris M, Miranda MA, Calvete C, Borràs D, Miquel M, Estrada R, Lucientes J (2009) Two years of Culicoides trap comparison in the Balearic Islands. Rev Elev Med Vet Pays Trop 62:81–180

    Google Scholar 

  • Dijkstra E, van der Ven IJK, Meiswinkel R, Hölzel DR, van Rijn PA, Meiswinkel R (2008) Culicoides chiopterus as a potential vector of bluetongue virus in Europe. Vet Rec 162:422

    Article  PubMed  CAS  Google Scholar 

  • Durand B, Zanella G, Biteau-Coroller F, Locatelli C, Baurier F, Simon C, Le Dréan E, Delaval J, Prengère E, Beauté V, Guis H (2010) Anatomy of bluetongue virus serotype 8 epizootic wave, France, 2007–2008. Emerg Infect Dis 16:1861–1868

    Article  PubMed  Google Scholar 

  • Enserink M (2008) Exotic disease of farm animals tests Europe’s responses. Science 319:710–711

    Article  PubMed  CAS  Google Scholar 

  • Eschbaumer M, Hoffmann B, Moss A, Savini G, Leone A, König P, Zemke J, Conraths F, Beer M (2009) Emergence of bluetongue virus serotype 6 in Europe-German field data and experimental infection of cattle. Vet Microbiol 143:189–195

    Article  PubMed  Google Scholar 

  • European Food Safety Authority (2007) Scientific Report of the Scientific Panel on Animal Health and Welfare on request from the Commission (EFSA-Q-2006-311) and EFSA self-mandate (EFSA-Q-2007-063) on bluetongue. Adopted by the AHAW panel on 27 April 2007. EFSA J 480:1–20

    Google Scholar 

  • Falconi C, López-Olvera JR, Gortázar C (2011) BTV infection in wild ruminants, with emphasis on red deer: a review. Vet Microbiol 151:209–219

    Article  PubMed  Google Scholar 

  • Fletcher D, Mackenzie D, Villouta D (2005) Modelling skewed data with many zeros: a simple approach combining ordinary and logistic regression. Environ Ecol Stat 12:45–54

    Article  Google Scholar 

  • Foxi C, Del Río G (2010) Larval habitats and seasonal abundance of Culicoides biting midges found in association with sheep in northern Sardinia, Italy. Med Vet Entomol 24:199–209

    Article  PubMed  CAS  Google Scholar 

  • García I, Napp S, Casal J, Perea A, Allepuz A, Alba A, Carbonero A, Arenas A (2009) Bluetongue epidemiology in wild ruminants from southern Spain. Eur J Wildl Res 55:173–178

    Article  Google Scholar 

  • Gerry AC, Sarto i Monteys V, Moreno Vidal JO, 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 46:615–624

    Article  PubMed  Google Scholar 

  • Goffredo M, Meiswinkel R (2004) Entomological surveillance of bluetongue in Italy: methods of capture, catch analysis and identification of Culicoides biting midges. Vet Ital 40:260–265

    PubMed  CAS  Google Scholar 

  • Hörbrand T, Geier M (2009) Monitoring of Culicoides at nine locations in Southern Germany (2007–2008). Parasitol Res 105:387–392

    Article  PubMed  Google Scholar 

  • Instituto Cartográfico de Andalucía (2005) Modelo Digital del Terreno de Andalucía: Relieve y Orografía a resolución 10 m. Junta de Andalucía, Sevilla

    Google Scholar 

  • Kaufmann C, Schaffner F, Mathis A (2009) Monitoring of biting midges (Culicoides spp.), the potential vectors of bluetongue virus, in the 12 climatic regions of Switzerland. Schw Arch Tierheilk 151:205–213

    Article  CAS  Google Scholar 

  • Kirkeby C, Bødker R, Stockmarr A, Enøe C (2010) Association between land cover and Culicoides (Diptera: Ceratopogonidae) breeding sites in four Danish cattle farms. Entomol Fennica 20:228–232

    Google Scholar 

  • Linden A, Grégoire F, Nahayo A, Hanrez D, Mousset B, Massart L, De Leeuw I, Vandemeulebroucke E, Vandenbussche F, De Clercq K (2010) Bluetongue virus in wild deer, Belgium, 2005–2008. Emerg Infect Dis 16:833–836

    PubMed  Google Scholar 

  • López-Olvera JR, Falconi C, Fernández-Pacheco P, Fernández-Pinero J, Sánchez MA, Palma A, Herruzo I, Vicente J, Jiménez-Clavero MA, Arias M, Sánchez-Vizcaíno JM, Gortázar C (2010) Experimental infection of European red deer (Cervus elaphus) with bluetongue virus serotypes 1 and 8. Vet Microbiol 145:148–152

    Article  PubMed  Google Scholar 

  • Lorca-Oró C, López-Olvera JR, Fernández-Sirera L, Solanes D, Navarro N, García-Bocanegra I, Lavín S, Domingo M, Pujols J (2012) Evaluation of the efficacy of commercial vaccines against bluetongue virus serotypes 1 and 8 in experimentally infected red deer (Cervus elaphus). Vet Microbiol 154:240–246

    Article  PubMed  Google Scholar 

  • Losson B, Mignon B, Paternostre J, Madder M, De Deken R, De Deken G, Deblauwe I, Fassotte C, Cors R, Defrance T, Delécoulle JC, Baldet T, Haubruge E, Francis F, Bortels J, Simonon G (2007) Biting midges overwintering in Belgium. Vet Rec 160:451–452

    Article  PubMed  Google Scholar 

  • Meiswinkel R, Venter GJ, Nevill EM (2004) Vectors: Culicoides spp. In: Coetzer JAW, Tustin RC (eds) Infectious diseases of livestock. Oxford University Press, Cape Town, pp 93–136

    Google Scholar 

  • Meiswinkel R, van Rijn P, Leijs P, Goffredo M (2007) Potential new Culicoides vector of bluetongue in northern Europe. Vet Rec 161:564–565

    Article  PubMed  CAS  Google Scholar 

  • Meiswinkel R, Goffredo M, Leijs P, Conte A (2008) The Culicoides ‘snapshot’: a novel approach used to assess vector densities widely and rapidly during the 2006 outbreak of bluetongue (BT) in The Netherlands. Prev Vet Med 87:98–118

    Article  PubMed  CAS  Google Scholar 

  • Mehlhorn H, Walldorf V, Klimpel S, Hahn B, Jaeger F, Eschweiler J (2007) First occurrence of Culicoides obsoletus-transmitted bluetongue virus epidemic in Central Europe. Parasitol Res 101:219–228

    Article  PubMed  Google Scholar 

  • Mehlhorn H, Walldorf V, Klimpel S, Schaub G, Kiel E, Focke R, Liebisch G, Liebisch A, Werner D, Bauer C, Clausen H, Bauer B, Geier M, Hörbrand T, Bätza HJ, Conraths FJ, Hoffmann B, Beer M (2009a) Bluetongue disease in Germany (2007–2008): monitoring of entomological aspects. Parasitol Res 105:313–319

    Article  PubMed  Google Scholar 

  • Mehlhorn H, Walldorf V, Klimpel S, Schmahl G, Saleh AQ, Walldorf U, Mehlhorn B, Bätza HJ (2009b) Entomological survey on vectors of bluetongue virus in Northrhine–Westfalia (Germany) during 2007 and 2008. Parasitol Res 105:321–329

    Article  PubMed  Google Scholar 

  • Mellor PS, Boorman J (1995) The transmission and geographical spread of African horse sickness and bluetongue viruses. Ann Trop Med Parasitol 89:1–15

    PubMed  CAS  Google Scholar 

  • Mellor PS, Pitzolis G (1979) Observations on breeding sites and light-traps collections of Culicoides during an outbreak of bluetongue in Çyprus. Bull Entomol Res 69:229–234

    Article  Google Scholar 

  • Mellor PS, Wittmann EJ (2002) Bluetongue virus in the Mediterranean Basin 1998-2001. Vet J 164:2037

    Article  Google Scholar 

  • Mellor PS, Tabachnick W, Baldet T, Baylis M, Bellis G, Calistri P, Delecolle JC, Gofredo M, Meiswinkel R, Mullens B, Scaramozzino P, Torina A, Venter G, White D (2004) Conclusions of working groups. Group 2. Vectors. Proceedings of the 3rd OIE Bluetongue International Symposium, 26-29 October 2003, Taornina, Italy. Vet Ital 40:715–717

    Google Scholar 

  • Nielsen SA, Nielsen BO, Chirico J (2010) Monitoring of biting midges (Diptera: Ceratopogonidae: Culicoides Latreille) on farms in Sweden during the emergence of the 2008 epidemic of bluetongue. Parasitol Res 106:1197–1203

    Article  PubMed  Google Scholar 

  • Nolan DV, Dallas JF, Piertney SB, Mordue AJ (2008) Incursion and range expansion of the bluetongue vector Culicoides imicola in the Mediterranean basin: a phylogeographic analysis. Med Vet Entomol 22:340–351

    Article  PubMed  CAS  Google Scholar 

  • Ortega MD, Mellor PS, Rawlings P, Pro MJ (1998) The seasonal and geographical distribution of Culicoides imicola. C. pulicaris group and C. obsoletus group biting midges in central and southern Spain. Arch Virol Suppl 14:85–91

    PubMed  CAS  Google Scholar 

  • Ortega MD, Holbrook FR, Lloyd JE (1999) Seasonal distribution and relationship to temperature and precipitation of the most abundant species of Culicoides in five provinces of Andalusia, Spain. J Am Mosq Control Assoc 15:391–399

    PubMed  CAS  Google Scholar 

  • Pérez JM, Granados JE, Soriguer RC, Fandos P, Márquez FJ, Crampe JP (2002) Distribution, status and conservation problems of the Spanish ibex, Capra pyrenaica (Mammalia, Artiodactyla). Mammal Rev 32:26–39

    Article  Google Scholar 

  • Price PW (1984) Insect ecology, 2nd edn. Wiley-Interscience, New York

    Google Scholar 

  • Probst C, Kampen H, Werner D, Gethmann J, Conraths FJ, Beer M (2009) Comparison of the efficacy of four light trap models for the collection of Culicoides biting midges in Germany. Rev Elev Med Vet Pays Trop 62:81–180

    Google Scholar 

  • Purse BV, Mellor PS, Rogers DJ, Samuel AR, Mertens PPC, Baylis M (2005) Climate change and the recent emergence of bluetongue in Europe. Nat Rev Microbiol 3:171–181

    Article  PubMed  CAS  Google Scholar 

  • Rawlings P (1996) A key based on wing patterns of biting midges (genus Culicoides Latreille–Diptera: Ceratopogonidae) in the Iberian Peninsula for use in epidemiological studies. Graellsia 52:57–71

    Article  Google Scholar 

  • R Development Core Team (2012) A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at http://www.R-project.org. Accessed 3 March, 2012

  • Rodríguez-Sánchez B, Iglesias-Martín I, Martínez-Avilés M, Sánchez-Vizcaíno JM (2008) Orbiviruses in the Mediterranean basin: updated epidemiological situation of bluetongue and new methods for the detection of BTV serotype 4. Transb Emerg Dis 55:205–214

    Article  Google Scholar 

  • Ruiz-Fons F, Reyes-García AR, Alcaide V, Gortázar C (2008) Spatial and temporal evolution of bluetongue virus in wild ruminants, Spain. Emerg Infect Dis 14:951–953

    Article  PubMed  Google Scholar 

  • Saegerman C, Berkvens D, Mellor PS (2008) Bluetongue epidemiology in the European Union. Emerg Infect Dis 14:539–544

    Article  PubMed  Google Scholar 

  • Santiago-Moreno J, Carvajal A, Astorga RJ, Coloma MA, Toledano-Díaz A, Gómez-Guillamón F, Salas-Vega R, López-Sebastián A (2011) Potential impact of disease transmissible by sperm on the establishment of Iberian ibex (Capra pyrenaica) genome resource banks. Eur J Wildl Res 57:211–216

    Article  Google Scholar 

  • Scheffer EG, Venter GJ, Labuschagne K, Page PC, Mullens BA, MacLachlan NJ, Osterrieder N, Guthrie AJ (2012) Comparison of two trapping methods for Culicoides biting midges and determination of African horse sickness virus prevalence in midge populations at Onderstepoort, South Africa. Vet Parasitol 185:265–273

    Article  PubMed  Google Scholar 

  • Sehnal P, Schweiger S, Schindler M, Anderle F, Schneemann Y (2008) Bluetongue: vector surveillance in Austria in 2007. Wien Klin Wochensch 120:34–39

    Article  Google Scholar 

  • Tschuor AC, Kaufmann C, Schaffner F, Mathis A (2009) Occurrence of biting midges (Culicoides spp.) at three different altitudes in an Alpine region of Switzerland. Schw Arch Tierheilk 151:215–221

    Article  CAS  Google Scholar 

  • Uslu U, Dik B (2010) Chemical characteristics of breeding sites of Culicoides species (Diptera: Ceratopogonidae). Vet Parasitol 169:178–184

    Article  PubMed  CAS  Google Scholar 

  • Veggiani Aybar CA, Dantur Juri MJ, Lizarralde de Grosso MS, Spinelli GR (2010) Species diversity and seasonal abundance of Culicoides biting midges in northwestern Argentina. Med Vet Entomol 24:95–98

    Article  Google Scholar 

  • Venter GJ, Hermanides KG (2006) Comparison of black and white light for collecting Culicoides imicola and other livestock-associated Culicoides species in South Africa. Vet Parasitol 142:383–385

    Article  PubMed  CAS  Google Scholar 

  • Venter GJ, Hermanides KG, Boikanyo SNB, Majatladi DM, Morey L (2009a) The effect of light trap height on the numbers of Culicoides midges collected under field conditions in South Africa. Vet Parasitol 166:343–345

    Article  PubMed  CAS  Google Scholar 

  • Venter GJ, Labuschagne K, Hermanides KG, Boikanyo SNB, Majatladi DM, Morey L (2009b) Comparison of the efficiency of five suction light traps under field conditions in South Africa for the collection of Culicoides species. Vet Parasitol 166:299–307

    Article  PubMed  CAS  Google Scholar 

  • Venter GJ, Labuschagne K, Hermanides I, Majatladi D, Boikanyo S (2009c) Culicoides trap comparison in South Africa. Rev Elev Med Vet Pays Trop 62:81–180

    Google 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 175:182–186

    Article  PubMed  CAS  Google Scholar 

  • Wigglesworth VB (1984) Insect physiology, 8th edn. Chapman and Hall, Oxford

    Google Scholar 

  • Wilson A, Mellor P (2008) Bluetongue in Europe: vectors, epidemiology and climate change. Parasitol Res 103(suppl 1):S69–S77

    Article  PubMed  Google Scholar 

  • Zientara S, Lecollinet S, Breard E, Sailleau C, Boireau P (2009) La fièvre du Nil Occidental et la fièvre catarrhale ovine, deux viroses en progression inattendue. Bull Acad Vét France 162:65–79

    Google Scholar 

  • Zimmer JY, Haubruge E, Francis F, Bortels J, Joie E, Simonon G, De Deken R, De Deken G, Deblauwe I, Madder M, Fassotte C, Cors R, Defrance T, Saegerman C, Thiry E, Mignon B, Paternostre J, Losson B, Kirschvink N (2008) Distribution of potential bluetongue vectors on Belgium farms. Vet Rec 162:700

    Article  PubMed  Google Scholar 

  • Zuur AF, Ieno EN, Smith GM (2007) Analysing ecological data. Springer, New York

    Google Scholar 

  • Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extension in ecology with R. Springer, New York

    Book  Google Scholar 

Download references

Acknowledgments

The authors wish to thank the Dirección General de la Producción Agraria y Ganadera, especially its General Director, Mrs. Judit Anda-Ugarte, for allowing the use of their captured data, as well as the staff of the public firm D.A.P., the coordinators of the monitoring program, for their help with the field work and Culicoides identification. We are also indebted to Dr. R. Meiswinkel for kindly supplying the relevant bibliographic references. E. Serrano is supported by a Beatriu de Pinós programme (BP-DGR 2011) of the Catalonian Science and Technology System, Spain. This work was partially supported by the Plan Andaluz de Investigación (Group RNM-118). The authors would also like to thank Michael Lockwood for his revision of the English language.

Author information

Authors and Affiliations

  1. Departamento de Biología Animal, Biología Vegetal y Ecología, Universidad de Jaén, Campus Las Lagunillas. s.n., 23071, Jaén, Spain

    Jesús M. Pérez & Juan A. García-Ballester

  2. Servei d´Ecopatologia de Fauna Salvatge, Departament de Medicina i Cirurgia Animals, Universitat Autònoma de Barcelona, 08193, Bellaterra, Barcelona, Spain

    Jorge R. López-Olvera & Emmanuel Serrano

  3. Estadística i Investigació Operativa, Departament de Matemàtica, Universitat de Lleida (UdL), 25298, Lleida, Spain

    Emmanuel Serrano

Authors
  1. Jesús M. Pérez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Juan A. García-Ballester
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jorge R. López-Olvera
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Emmanuel Serrano
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jesús M. Pérez.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pérez, J.M., García-Ballester, J.A., López-Olvera, J.R. et al. Monitoring bluetongue virus vectors in Andalusia (SW Europe): Culicoides species composition and factors affecting capture rates of the biting midge Culicoides imicola . Parasitol Res 111, 1267–1275 (2012). https://doi.org/10.1007/s00436-012-2961-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-012-2961-3

Keywords

Search

Navigation