Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter October 24, 2016

First insights into indoor and outdoor Culicoides activity related to the risk period for Bluetongue virus transmission in Eastern Slovakia

Adela Sarvašová EMAIL logo , Alica Kočišová , Erika Liptáková , Helena Hiavatá and Bruno Mathieu
From the journal Acta Parasitologica

Abstract

The epizootic of Bluetongue virus (BTV) throughout Europe in 2006 revealed insufficient knowledge regarding seasonal activities, endo/exophilic and endo/exophagic behaviour of the species of the Culicoides genus (Diptera: Ceratopogonidae). Although several studies have been carried out in Western Europe, bringing new knowledge of the above mentioned topics, there was still a gap to fill in Central Europe. Therefore, this study investigated seasonal variations in the indoor/outdoor Culicoides activity observed in the south-eastern Slovakia from 2012 to 2014, using a light-trapping method. In total, 52,741 Culicoides were collected and identified; majority of them were caught outdoors (82.6%), with the highest activity period being mid-June. The C. obsoletus/C. scoticus and C.punctatus species predominated, altogether representing 88.8 and 94.1% of the total indoor and outdoor collections, respectively. Positive correlation was observed between the temperature and the abundance, whereas no correlation with other studied factors was detected. In autumn, Culicoides activity was observed outdoors at temperatures ranging between-1.5°C and 9.3°C, whereas the indoor activity was detected at temperatures ranging between-3.9°C and 0°C. This demonstrated that the most significant BTV vectors in the studied area are C. obsoletus/C. scoticus. The C. dewulfi and C. chiopterus vectors appeared to be of lower significance. The period with the highest risk of the BTV transmission in Eastern Slovakia appeared to be mid-June. The autumnal Culicoides activity inside the cowsheds may be important for the assessment of virus overwintering. This study is the first to provide the data on indoor/outdoor behaviour of biting midges in Slovakia.

Acknowledgements

This research was supported by grant VEGA No. 1/0080/15 (share 0.7), the basic research was provided by the National Referential Laboratory for Pesticides of the University of Veterinary Medicine and Pharmacy in Kosice, and we wish to thank the "Centre of Excellence for Parasitology" Project (ITMS code: 26220120022) for providing support to the operational program for the Research and Development, funded by the European Regional Development Fund.

References

Ander M., Meiswinkel R., Chirico J. 2012. Seasonal dynamics of biting midges (Diptera: Ceratopogonidae: Culicoides), the potential vectors of Bluetongue virus, in Sweden. Veterinary Parasitology 184, 59-67. 10.1016/j.vetpar.2011.08.009Search in Google Scholar PubMed

Baldet T., Delécolle J.C., Cêtre-Sossah C., Mathieu B., Meiswinkel R., Gerbier G. 2008. Indoor activity of Culicoides associated with livestock in the Bluetongue virus (BTV) affected region of northern France during autumn 2006. Preventive Veterinary Medicine 87, 84-97. 10.1016/j.prevetmed.2008.06.014 "Search in Google Scholar

Balenghien T., Cetre-Sossah C., Grillet C., Delécolle J.C., Mathieu B., Baldet T. 2008. Diurnal activity of potential bluetongue vectors in northern Europe. Veterinary Record 162, 323-32410.1136/vr.162.10.323-bSearch in Google Scholar PubMed

Balenghien T., Delécolle J.-C., Setier-Rio M.-L., Rakotaoarivony I., Allène X., Venail R., Delécolle D., Lhoir J., Gardés L., Chav-ernac D. 2011. Bluetongue - report on entomological surveillance in France in 2010. Bulletin Epidémiologique Hebdomadaire 46, 26-31Search in Google Scholar

Baylis M., Parkin H., Keppel K., Carpenter S., Mellor P.S., McIntyre K.M. 2010. Evaluation of housing as a means to protect cattle from Culicoides biting midges, the vectors of Bluetongue virus. Medical and Veterinary Entomology 24, 38-45. 10.1111/j.1365-2915.2009.00842.xSearch in Google Scholar PubMed

Caracappa S., Torina A., Guercio A., Vitale F., Calabro A., Purpari G., Ferrantelli V., Vitale M., Mellor P.S. 2003. Identification of a novel Bluetongue virus vector species of Culicoides in Sicily. Veterinary Record 153, 71-74. 10.1136/vr.153.3.71Search in Google Scholar PubMed

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? Journal of Applied Ecology 45, 1237-1245. 10.1111/j.1365-2664.2008.01511.xSearch in Google Scholar

Clausen P.-H., Stephan A., Bartsch S., Jandowsky A., HoffmannKöhler P., Schein E., Mehlitz D., Bauer B. 2009. Seasonal dy-namics of biting midges (Diptera: Ceratopogonidae, Culicoides spp.) on dairy farms of Central Germany during the 2007/2008 epidemic of bluetongue. Parasitology Research 105, 381-386. 10.1007/s00436-009-1417-xSearch in Google Scholar PubMed

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. Veterinary Parasitology 150, 333-344. 10.1016/j.vetpar.2007.09.021Search in Google Scholar PubMed

De Liberato C., Purse B.V., Goffredo M., Scholl F., Scaramozzino P. 2003. Geographical and seasonal distribution of the Bluetongue virus vector, Culicoides imicola, in central Italy. Medical and Veterinary Entomology 17, 388-394. 10.1111/j.1365-2915.2003.00456.xSearch in Google Scholar PubMed

De Regge N., Deblauwe I., De Deken R., Vantieghem P., Madder M., Geysen D., Smeets F., Losson B., van den Berg T., Cay A.B. 2012. Detection of Schmallenberg virus in different Culicoides spp. by real-time RT-PCR. Transboundary and Emerging Diseases 59, 471-475. 10.1111/tbed.12000Search in Google Scholar PubMed

Delécolle J.-C. 1985. New contribution to the systematic and icono-graphic study of the species of the Culicoides genus (Diptera : Ceratopogonidae) from the North-East of France. Université Louis Pasteur de Strasbourg, Strasbourg. (In French)Search in Google Scholar

Dijkstra E., van der Ven I.J.K., Meiswinkel R., Hölzel D.R., Van Rijn P.A., Meiswinkel R. 2008. Culicoides chiopterus as a potential vector of Bluetongue virus in Europe. Veterinary Record 162, 422. 10.1136/vr.162.13.422-aSearch in Google Scholar PubMed

Dyce A.L. 1969. The recognition of nulliparous and parous Culicoides (Diptera: Ceratopogonidae) without dissection. Journal of Australian Entomological Society 8, 11-15. 10.1111/j.1440-6055.1969.tb00727.xSearch in Google Scholar

Goffredo M., Catalani M., Federici V., Portanti O., Marini V., Mancini G., Quaglia M., Santilli A., Teodori L., Savini G. 2015. Vector species of Culicoides midges implicated in the 2012 2014 Bluetongue epidemics in Italy. Veterinaria Italiana 51, 131-138. 10.12834/VetIt.771.3854.1Search in Google Scholar PubMed

Lackovâ Z., Bires J., Smarzik M., Tinâk M. 2012. Clinical and Laboratory Picture in Calves in Rearing with Incidence Bluetongue. The Open Agriculture Journal 6, 74-78. 10.2174/1874331501206010074Search in Google Scholar

Larska M., Lechowski L., Grochowska M., Zmudzinski J.F. 2013. Detection of the Schmallenberg virus in nulliparous Culi-coides obsoletus/scoticus complex and C. punctatus-the possibility of transovarial virus transmission in the midge population and of a new vector. Veterinary Microbiology166, 467-473. 10.1016/j.vetmic.2013.07.015Search in Google Scholar PubMed

Losson B., Mignon B., Paternostre J., Madder M., De Deken R., De Deken G., Deblauwe I., Fassotte C., Cors R., Defrance T., Delécolle J.-C., Baldet T., Haubruge E., Frédéric F., Bortels J., Simonon G. 2007. Biting midges overwintering in Belgium. Veterinary Record 160, 451-452.10.1136/vr.160.13.451-bSearch in Google Scholar PubMed

Mathieu B., Cêtre-Sossah C., Garros C., Chavernac D., Balenghien T., Carpenter S., Setier-Rio M.-L., Vignes-Lebbe R., Ung V., Candolfi E., Delécolle J.-C., 2012. Development and validation of IIKC: an interactive identification key for Culicoides (Diptera: Ceratopogonidae) females from the Western Palaearctic region. Parasites & Vectors 5, 137. 10.1186/1756-3305-5-137Search in Google Scholar PubMed PubMed Central

Mehlhorn H., Walldorf V., Klimpel S., Jahn B., Jaeger F., Eschweiler J., Hoffmann B., Beer M. 2007. First occurrence of Culicoides obsoletus-transmitted Bluetongue virus epidemic in Central Europe. Parasitology Research 101, 219-228. 10.1007/s00436-007-0519-6Search in Google Scholar PubMed

Meiswinkel R., Goffredo M., Dijkstra E.G., van der Ven I.J., Baldet T., Elbers A. 2008. Endophily in Culicoides associated with BTV-infected cattle in the province of Limburg, south-eastern Netherlands, 2006. Preventive Veterinary Medicine 87, 182195. 10.1016/j.prevetmed.2008.06.008Search in Google Scholar PubMed

Meiswinkel R., van Rijn P., Leijs P., Goffredo M. 2007. Potential new Culicoides vector of Bluetongue virus in northern Europe. Veterinary Record 161, 564-565. 10.1136/vr.161.16.564Search in Google Scholar PubMed

Mellor P.S., Boorman J., Baylis M. 2000. Culicoides biting midges: their role as arbovirus vectors. Annual Review of Entomology 45, 307-340. 10.1146/annurev.ento.45.1.307Search in Google Scholar PubMed

Ninio C., Augot D., Dufour B., Depaquit J. 2011. Emergence of Culicoides obsoletus from indoor and outdoor breeding sites. Veterinary Parasitology 183, 125-129. 10.1016/j.vetpar.2011.07.020Search in Google Scholar PubMed

ProMED-mail 2015. Bluetongue - Europe (11): France, serotype 8, Romania, Hungary, serotype 4, spread. ProMED-mail 13 Oct: 20151014.3715855 <<http://www.promedmail.org>. Accessed 13 Oct 2015Search in Google Scholar

Râdrovâ J., Mrackovâ M., Galkovâ Z., Lamka J., Racka K., Bartâk P., Votypka J. 2016. Seasonal Dynamics, Parity Rate, and Composition of Culicoides (Diptera: Ceratopogonidae) Occurring in the Vicinity of Wild and Domestic Ruminants in the Czech Republic. Journal of Medical Entomology 53, 416424. 10.1093/jme/tjv197Search in Google Scholar PubMed

Romon P., Higuera M., Delecolle J.C., Baldet T., Aduriz G., Goldarazena A. 2012. Phenology and attraction of potential Culicoides vectors of Bluetongue virus in Basque Country (northern Spain). Veterinary Parasitology 186, 415-424. 10.1016/j.vetpar.2011.11.023Search in Google Scholar PubMed

Sarvasovâ A. 2014. Biodiversity, competence and epidemiological role of selected species of blood sucking diptera (Diptera: Cerato-pogonidae) of Eastern Slovakia. (PhD. thesis). University of Veterinary Medicine and Pharmacy in Kosice, SlovakiaSearch in Google Scholar

Sarvasovâ A., Goffredo M., Sopoliga I., Savini G., Kocisovâ A. 2014a. Culicoides midges (Diptera: Ceratopogonidae) as vectors of orbiviruses in Slovakia. Veterinaria Italiana 50, 203212. 10.12834/VetIt.40.1916.8Search in Google Scholar PubMed

Sarvasovâ A., Kocisovâ A., Halân M., Delécolle J.-C., Mathieu B. 2014b. Morphological and molecular analysis of the genus Culicoides (Diptera: Ceratopogonidae) in Slovakia with five new records. Zootaxa 3872, 541-560. DOI:http://dx.DOI.org/10.11646/zootaxa.3872.5.610.11646/zootaxa.3872.5.6Search in Google Scholar PubMed

Savini G., Goffredo M., Monaco F., Di Gennaro A., Cafiero M.A., Baldi L., de Santis P., Meiswinkel R., Caporale V. 2005. Blue-tongue virus isolations from midges belonging to the Obsole-tus complex (Culicoides, Diptera: Ceratopogonidae) in Italy. Veterinary Record 157, 133-139.10.1136/vr.157.5.133Search in Google Scholar PubMed

Savini G., Goffredo M., Monaco F., Di Gennaro A., de Santis P., Meiswinkel R., Caporale V. 2004. The isolation of Bluetongue virus from field populations of the Obsoletus Complex in central Italy. Veterinaria Italiana 40, 286-291Search in Google Scholar

Sehnal P., Schweiger S., Schindler M., Anderle F., Schneemann Y. 2008. Bluetongue: Vector surveillance in Austria in 2007. Wiener Klinische Wochenschrift 120, 34-39. 10.1007/ s00508-008-1073-7Search in Google Scholar

Uslu U., Dik B. 2010. Chemical characteristics of breeding sites of Culicoides species (Diptera: Ceratopogonidae). Veterinary Parasitology 169, 178-184. 10.1016/j.vetpar.2009.12.007Search in Google Scholar PubMed

Vanbinst T., Vandenbussche F., Vandemeulebroucke E., De Leeuw I., Deblauwe I., De Deken G., Madder M., Haubruge E., Losson B., De Clercq K. 2009. Bluetongue virus detection by real-time RT-PCR in Culicoides captured during the 2006 epizootic in Belgium and development of an internal control. Transboundary and Emerging Diseases 56, 170-177. 10.1111/j.1865-1682.2009.01077.xSearch in Google Scholar PubMed

Viennet E., Garros C., Lancelot R., Allene X., Gardes L., Rako-toarivony I., Crochet D., Delecolle J.C., Moulia C., Baldet T., Balenghien T. 2011. Assessment of vector/host contact: comparison of animal-baited traps and UV-light/suction trap for collecting Culicoides biting midges (Diptera: Ceratopogo-nidae), vectors of Orbiviruses. Parasites & Vectors 4, 119. 10.1186/1756-3305-4-119Search in Google Scholar PubMed PubMed Central

Viennet E., Garros C., Rakotoarivony I., Allène X., Gardés L., Lhoir J., Fuentes I., Venail R., Crochet D., Lancelot R., Riou M., Moulia C., Baldet T., Balenghien T. 2012. Host-seeking activity of Bluetongue virus vectors: endo/exophagy and circa-dian rhythm of Culicoides in Western Europe. PLoS ONE 7, e48120. 10.1371/journal.pone.0048120Search in Google Scholar PubMed PubMed Central

Zimmer, J.-Y. Haubruge E., Francis F., Bortels J., Simonon G., Losson B., Mignon B., Paternostre J., De Deken R., De Deken G., Deblauwe I., Fassotte C., Cors R., Defrance T. 2008. Breeding sites of bluetongue vectors in northern Europe. Veterinary Record 162, 13110.1136/vr.162.4.131Search in Google Scholar PubMed

Zimmer J.-Y., Saegerman C., Losson B., Haubruge E. 2010. Breeding Sites of Bluetongue Virus Vectors, Belgium. Emerging In-fectious Diseases 16, 575-576. 10.3201/eid1603.091311Search in Google Scholar PubMed PubMed Central

Supplements

Table SI

Comparison of biodiversity and abundance between indoors and outdoors collected Culicoides in 2012. Species are ranked in decreasing order of abundance and percentages of parous (%P) and blood-fed (%B) females

RankSpeciesTotalMean catch% totalMaximum catch% P% BSex ratio
1C. obsoletus/scoticus30734.162.114642.1715.64.07
2C. punctatus15116.830.69434.611.20
3C. newsteadi242.74.94236.454.20
4C. pulicaris40.40.84
5C. subfasciipennis30.30.6
6C. riethi20.20.4
7C. lupicaris10.10.2
8C. nubeculosus10.10.2
9C. salinarius10.10.2
Total indoor49454.9100
RankSpeciesTotalMean catch% totalMaximum catch% P% BSex ratio
1C.obsoletus/scoticus1,325147.242.2579832.282.050.3
2C. punctatus83292.426.5377458.35.170
3C. riethi57163.418.21463970.555
4C. salinarius9210.22.936210002.2
5C. circumscriptus9210.22.93469900
6C. newsteadi90102.871136.42.20
7C. nubeculosus384.21.211885015
8C. pulicaris242.70.771036.42.20
9C. manchuriensis161.80.51137500
10C. festivipennis151.70.486100015.4
11C. furcillatus910.29
12C. subfasciipennis80.90.26
13C. tauricus80.90.26
14C. picturatus60.70.19
15C. fasciipennis30.30.10
16C. alazanicus30.30.10
17C. lupicaris20.20.06
18C. gejgelensis10.10.03
19C. kibunensis10.10.03
Total outdoor3,136348.4100
Table SII

Comparison of biodiversity and abundance between indoors and outdoors collected Culicoides in 2013. Species are ranked in decreasing order of abundance and percentages of parous (%P) and blood-fed (%B) females

RankSpeciesTotalMean catch% totalMaximum catch% P% BSex ratio
1C. punctatus2,566285.150.221,52244.1200.6
2C.obsoletus/scoticus2,251250.144.057125220.611.6
3C. newsteadi15417.13.015829.724.80
4C. pulicaris606.71.171654.2200
5C. subfasciipennis232.60.451442.117.40
6C. fasciipennis121.30.231011.1750
7C. griseidorsum101.10.20675600
8C. riethi70.80.14
9C. parroti50.60.10
10C. picturatus50.60.10
11C. furcillatus50.60.10
12C. nubeculosus40.40.08
13C. lupicaris20.20.04
14C. achrayi20.20.04
15C. puncticollis20.20.04
16C. manchuriensis10.10.02
17C. salinarius10.10.02
Total indoor5,110567.8100
RankSpeciesTotalMean catch% totalMaximum catch% P% BSex ratio
1C. punctatus18,6791436.869.6215,39343.40.530.09
2C.obsoletus/scoticus5,601430.820.883,05933.60.650.27
3C. riethi487371.8211186.861.2430.6
4C. newsteadi48133.31.7942238.0300.62
5C. puncticollis457301.7032298.8505.5
6C. salinarius21716.70.8112798.200
7C. pulicaris182140.686254.700.55
8C. circumscriptus17113.20.646893.903.6
9C. parroti/stigma1158.80.4310260.61.83.6
10C. fasciipennis927.10.348630.81.090
11C. furcillatus846.50.317839.300
12C. subfasciipennis745.70.286161.61.40
13C. picturatus342.60.132932.309.7
14C. nubeculosus412.40.153087.1032.3
15C. festivipennis302.30.111410000
16C. slovacus/tauricus241.80.09227500
17C. griseidorsum241.80.091966.700
18C. manchuriensis100.80.0493000
19C. achrayi80.60.03
20C. odiatus70.50.03
21C. pictipennis40.30.01
22C. lupicaris30.20.01
23C. kibunensis10.080.00
24C. chiopterus10.080.00
25C. dewulfi10.080.00
26C. alazanicus10.080.00
27C. riouxi10.080.00
Total outdoor26,8302058.3100
Table SIII

Comparison of biodiversity and abundance between indoors and outdoors collected Culicoides in 2014. Species are ranked in decreasing order of abundance and percentages of parous (%P) and blood-fed (%B) females

RankSpeciesTotalMean catch% totalMaximum catch% P% BSex ratio
1C. obsoletus/scoticus3,187227.690.0359754.214.63.8
2C. punctatus14210.14.013943.48.50.71
3C. newsteadi1017.22.852526.517.80
4C. pulicaris634.51.783036.74.80
5C. chiopterus100.70.28
6C. nubeculosus80.60.23
7C. salinarius60.40.17
8C. slovacus60.40.17
9C. griseidorsum40.30.11
10C. subfasciipennis30.210.08
11C. parroti20.140.06
12C. fasciipennis20.140.06
13C. riethi10.070.03
14C. lupicaris10.070.03
15C. puncticollis10.070.03
16C. picturatus10.070.03
17C. festivipennis10.070.03
18C. furcilatus10.070.03
Total indoor3,540252100
RankSpeciesTotalMean catch% totalMaximum catch% P% BSex ratio
1C.obsoletus/scoticus11,235802.582.423,35439.11.80.11
2C. punctatus1,03974.27.6243040.91.90.29
3C. newsteadi57140.84.199020.21.20.18
4C. pulicaris39027.62.8621540.400.26
5C. salinarius1379.81.014310000
6C. riethi674.80.493785.708
7C. circumscriptus584.140.433598.300
8C. furcilatus322.30.232543.800
9C. nubeculosus221.570.16794.45.2615.8
10C. puncticollis120.860.09787.52020
11C. tauricus/slovacus90.640.07
12C. stigma/parroti80.570.06
13C. festivipennis80.570.06
14C. achrayi70.50.05
15C. chiopterus70.50.05
16C. griseidorsum50.360.04
17C. subfasciipennis50.350.04
18C. manchuriensis40.290.03
19C. lupicaris30.20.02
20C. fasciipennis30.210.02
21C. fasciipennis30.210.02
22C. simulator20.140.01
23C. pictipennis20.140.01
24C. odiatus10.070.01
25C. riouxi10.070.01
Total outdoor13,631973.6100
Table SIV a

Kendall's correlation coefficients of dependencies between the Culicoides activity in 2012, 2013 and 2014, and the maximum (Tmax), mean (Tavar) and minimum (Tmin) temperatures

Kendalls tau_bTmaxTaverTmin
2012Correlation coefficient0.556*0.535*0.556*
Sig. (2-tailed)0.0370.0460.037
2013Correlation coefficient0.718**0.769**0.658**
Sig. (2-tailed)0.010.0000.002
2014Correlation coefficient0.398*0.508*0.575**
Sig. (2-tailed)0.0480.0120.004
Table SIV b

Kendall's correlation coefficients of dependencies between the Culicoides activity in 2012, 2013 and 2014, and the humidity, wind speed and rainfall

Kendalls tau_bHumidityWind speedRainfall
2012Correlation coefficient-0.423-0.2100.340
Sig. (2-tailed)0.1160.4510.225
2013Correlation coefficient0.116-0.2070.071
Sig. (2-tailed)0.5820.3470.768
2014Correlation coefficient-0.1550.151-0.105
Sig. (2-tailed)0.4430.4680.644
Fig. S1a Scatter charts showing correlation between Culicoides numbers collected outdoors and temperature
Fig. S1a

Scatter charts showing correlation between Culicoides numbers collected outdoors and temperature

Fig. S1 b Scatter chart showing no significant correlation between the Culicoides numbers collected outdoors and humidity, wind speed, or rainfall
Fig. S1 b

Scatter chart showing no significant correlation between the Culicoides numbers collected outdoors and humidity, wind speed, or rainfall

Received: 2016-1-25
Revised: 2016-6-17
Accepted: 2016-6-21
Published Online: 2016-10-24
Published in Print: 2016-12-1

© 2016 W. Stefański Institute of Parasitology, PAS

Downloaded on 30.11.2022 from frontend.live.degruyter.dgbricks.com/document/doi/10.1515/ap-2016-0103/html
Scroll Up Arrow