First insights into indoor and outdoor Culicoides activity related to the risk period for Bluetongue virus transmission in Eastern Slovakia
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
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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
| Rank | Species | Total | Mean catch | % total | Maximum catch | % P | % B | Sex ratio |
|---|---|---|---|---|---|---|---|---|
| 1 | C. obsoletus/scoticus | 307 | 34.1 | 62.1 | 146 | 42.17 | 15.6 | 4.07 |
| 2 | C. punctatus | 151 | 16.8 | 30.6 | 94 | 34.6 | 11.2 | 0 |
| 3 | C. newsteadi | 24 | 2.7 | 4.9 | 42 | 36.4 | 54.2 | 0 |
| 4 | C. pulicaris | 4 | 0.4 | 0.8 | 4 | |||
| 5 | C. subfasciipennis | 3 | 0.3 | 0.6 | ||||
| 6 | C. riethi | 2 | 0.2 | 0.4 | ||||
| 7 | C. lupicaris | 1 | 0.1 | 0.2 | ||||
| 8 | C. nubeculosus | 1 | 0.1 | 0.2 | ||||
| 9 | C. salinarius | 1 | 0.1 | 0.2 | ||||
| Total indoor | 494 | 54.9 | 100 |
| Rank | Species | Total | Mean catch | % total | Maximum catch | % P | % B | Sex ratio |
|---|---|---|---|---|---|---|---|---|
| 1 | C.obsoletus/scoticus | 1,325 | 147.2 | 42.25 | 798 | 32.28 | 2.05 | 0.3 |
| 2 | C. punctatus | 832 | 92.4 | 26.53 | 774 | 58.3 | 5.17 | 0 |
| 3 | C. riethi | 571 | 63.4 | 18.21 | 463 | 97 | 0.55 | 5 |
| 4 | C. salinarius | 92 | 10.2 | 2.93 | 62 | 100 | 0 | 2.2 |
| 5 | C. circumscriptus | 92 | 10.2 | 2.93 | 46 | 99 | 0 | 0 |
| 6 | C. newsteadi | 90 | 10 | 2.87 | 11 | 36.4 | 2.2 | 0 |
| 7 | C. nubeculosus | 38 | 4.2 | 1.21 | 18 | 85 | 0 | 15 |
| 8 | C. pulicaris | 24 | 2.7 | 0.77 | 10 | 36.4 | 2.2 | 0 |
| 9 | C. manchuriensis | 16 | 1.8 | 0.51 | 13 | 75 | 0 | 0 |
| 10 | C. festivipennis | 15 | 1.7 | 0.48 | 6 | 100 | 0 | 15.4 |
| 11 | C. furcillatus | 9 | 1 | 0.29 | ||||
| 12 | C. subfasciipennis | 8 | 0.9 | 0.26 | ||||
| 13 | C. tauricus | 8 | 0.9 | 0.26 | ||||
| 14 | C. picturatus | 6 | 0.7 | 0.19 | ||||
| 15 | C. fasciipennis | 3 | 0.3 | 0.10 | ||||
| 16 | C. alazanicus | 3 | 0.3 | 0.10 | ||||
| 17 | C. lupicaris | 2 | 0.2 | 0.06 | ||||
| 18 | C. gejgelensis | 1 | 0.1 | 0.03 | ||||
| 19 | C. kibunensis | 1 | 0.1 | 0.03 | ||||
| Total outdoor | 3,136 | 348.4 | 100 |
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
| Rank | Species | Total | Mean catch | % total | Maximum catch | % P | % B | Sex ratio |
|---|---|---|---|---|---|---|---|---|
| 1 | C. punctatus | 2,566 | 285.1 | 50.22 | 1,522 | 44.1 | 20 | 0.6 |
| 2 | C.obsoletus/scoticus | 2,251 | 250.1 | 44.05 | 712 | 52 | 20.6 | 11.6 |
| 3 | C. newsteadi | 154 | 17.1 | 3.01 | 58 | 29.7 | 24.8 | 0 |
| 4 | C. pulicaris | 60 | 6.7 | 1.17 | 16 | 54.2 | 20 | 0 |
| 5 | C. subfasciipennis | 23 | 2.6 | 0.45 | 14 | 42.1 | 17.4 | 0 |
| 6 | C. fasciipennis | 12 | 1.3 | 0.23 | 10 | 11.1 | 75 | 0 |
| 7 | C. griseidorsum | 10 | 1.1 | 0.20 | 6 | 75 | 60 | 0 |
| 8 | C. riethi | 7 | 0.8 | 0.14 | ||||
| 9 | C. parroti | 5 | 0.6 | 0.10 | ||||
| 10 | C. picturatus | 5 | 0.6 | 0.10 | ||||
| 11 | C. furcillatus | 5 | 0.6 | 0.10 | ||||
| 12 | C. nubeculosus | 4 | 0.4 | 0.08 | ||||
| 13 | C. lupicaris | 2 | 0.2 | 0.04 | ||||
| 14 | C. achrayi | 2 | 0.2 | 0.04 | ||||
| 15 | C. puncticollis | 2 | 0.2 | 0.04 | ||||
| 16 | C. manchuriensis | 1 | 0.1 | 0.02 | ||||
| 17 | C. salinarius | 1 | 0.1 | 0.02 | ||||
| Total indoor | 5,110 | 567.8 | 100 |
| Rank | Species | Total | Mean catch | % total | Maximum catch | % P | % B | Sex ratio |
|---|---|---|---|---|---|---|---|---|
| 1 | C. punctatus | 18,679 | 1436.8 | 69.62 | 15,393 | 43.4 | 0.53 | 0.09 |
| 2 | C.obsoletus/scoticus | 5,601 | 430.8 | 20.88 | 3,059 | 33.6 | 0.65 | 0.27 |
| 3 | C. riethi | 487 | 37 | 1.82 | 111 | 86.86 | 1.24 | 30.6 |
| 4 | C. newsteadi | 481 | 33.3 | 1.79 | 422 | 38.03 | 0 | 0.62 |
| 5 | C. puncticollis | 457 | 30 | 1.70 | 322 | 98.85 | 0 | 5.5 |
| 6 | C. salinarius | 217 | 16.7 | 0.81 | 127 | 98.2 | 0 | 0 |
| 7 | C. pulicaris | 182 | 14 | 0.68 | 62 | 54.7 | 0 | 0.55 |
| 8 | C. circumscriptus | 171 | 13.2 | 0.64 | 68 | 93.9 | 0 | 3.6 |
| 9 | C. parroti/stigma | 115 | 8.8 | 0.43 | 102 | 60.6 | 1.8 | 3.6 |
| 10 | C. fasciipennis | 92 | 7.1 | 0.34 | 86 | 30.8 | 1.09 | 0 |
| 11 | C. furcillatus | 84 | 6.5 | 0.31 | 78 | 39.3 | 0 | 0 |
| 12 | C. subfasciipennis | 74 | 5.7 | 0.28 | 61 | 61.6 | 1.4 | 0 |
| 13 | C. picturatus | 34 | 2.6 | 0.13 | 29 | 32.3 | 0 | 9.7 |
| 14 | C. nubeculosus | 41 | 2.4 | 0.15 | 30 | 87.1 | 0 | 32.3 |
| 15 | C. festivipennis | 30 | 2.3 | 0.11 | 14 | 100 | 0 | 0 |
| 16 | C. slovacus/tauricus | 24 | 1.8 | 0.09 | 22 | 75 | 0 | 0 |
| 17 | C. griseidorsum | 24 | 1.8 | 0.09 | 19 | 66.7 | 0 | 0 |
| 18 | C. manchuriensis | 10 | 0.8 | 0.04 | 9 | 30 | 0 | 0 |
| 19 | C. achrayi | 8 | 0.6 | 0.03 | ||||
| 20 | C. odiatus | 7 | 0.5 | 0.03 | ||||
| 21 | C. pictipennis | 4 | 0.3 | 0.01 | ||||
| 22 | C. lupicaris | 3 | 0.2 | 0.01 | ||||
| 23 | C. kibunensis | 1 | 0.08 | 0.00 | ||||
| 24 | C. chiopterus | 1 | 0.08 | 0.00 | ||||
| 25 | C. dewulfi | 1 | 0.08 | 0.00 | ||||
| 26 | C. alazanicus | 1 | 0.08 | 0.00 | ||||
| 27 | C. riouxi | 1 | 0.08 | 0.00 | ||||
| Total outdoor | 26,830 | 2058.3 | 100 |
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
| Rank | Species | Total | Mean catch | % total | Maximum catch | % P | % B | Sex ratio |
|---|---|---|---|---|---|---|---|---|
| 1 | C. obsoletus/scoticus | 3,187 | 227.6 | 90.03 | 597 | 54.2 | 14.6 | 3.8 |
| 2 | C. punctatus | 142 | 10.1 | 4.01 | 39 | 43.4 | 8.5 | 0.71 |
| 3 | C. newsteadi | 101 | 7.2 | 2.85 | 25 | 26.5 | 17.8 | 0 |
| 4 | C. pulicaris | 63 | 4.5 | 1.78 | 30 | 36.7 | 4.8 | 0 |
| 5 | C. chiopterus | 10 | 0.7 | 0.28 | ||||
| 6 | C. nubeculosus | 8 | 0.6 | 0.23 | ||||
| 7 | C. salinarius | 6 | 0.4 | 0.17 | ||||
| 8 | C. slovacus | 6 | 0.4 | 0.17 | ||||
| 9 | C. griseidorsum | 4 | 0.3 | 0.11 | ||||
| 10 | C. subfasciipennis | 3 | 0.21 | 0.08 | ||||
| 11 | C. parroti | 2 | 0.14 | 0.06 | ||||
| 12 | C. fasciipennis | 2 | 0.14 | 0.06 | ||||
| 13 | C. riethi | 1 | 0.07 | 0.03 | ||||
| 14 | C. lupicaris | 1 | 0.07 | 0.03 | ||||
| 15 | C. puncticollis | 1 | 0.07 | 0.03 | ||||
| 16 | C. picturatus | 1 | 0.07 | 0.03 | ||||
| 17 | C. festivipennis | 1 | 0.07 | 0.03 | ||||
| 18 | C. furcilatus | 1 | 0.07 | 0.03 | ||||
| Total indoor | 3,540 | 252 | 100 |
| Rank | Species | Total | Mean catch | % total | Maximum catch | % P | % B | Sex ratio |
|---|---|---|---|---|---|---|---|---|
| 1 | C.obsoletus/scoticus | 11,235 | 802.5 | 82.42 | 3,354 | 39.1 | 1.8 | 0.11 |
| 2 | C. punctatus | 1,039 | 74.2 | 7.62 | 430 | 40.9 | 1.9 | 0.29 |
| 3 | C. newsteadi | 571 | 40.8 | 4.19 | 90 | 20.2 | 1.2 | 0.18 |
| 4 | C. pulicaris | 390 | 27.6 | 2.86 | 215 | 40.4 | 0 | 0.26 |
| 5 | C. salinarius | 137 | 9.8 | 1.01 | 43 | 100 | 0 | 0 |
| 6 | C. riethi | 67 | 4.8 | 0.49 | 37 | 85.7 | 0 | 8 |
| 7 | C. circumscriptus | 58 | 4.14 | 0.43 | 35 | 98.3 | 0 | 0 |
| 8 | C. furcilatus | 32 | 2.3 | 0.23 | 25 | 43.8 | 0 | 0 |
| 9 | C. nubeculosus | 22 | 1.57 | 0.16 | 7 | 94.4 | 5.26 | 15.8 |
| 10 | C. puncticollis | 12 | 0.86 | 0.09 | 7 | 87.5 | 20 | 20 |
| 11 | C. tauricus/slovacus | 9 | 0.64 | 0.07 | ||||
| 12 | C. stigma/parroti | 8 | 0.57 | 0.06 | ||||
| 13 | C. festivipennis | 8 | 0.57 | 0.06 | ||||
| 14 | C. achrayi | 7 | 0.5 | 0.05 | ||||
| 15 | C. chiopterus | 7 | 0.5 | 0.05 | ||||
| 16 | C. griseidorsum | 5 | 0.36 | 0.04 | ||||
| 17 | C. subfasciipennis | 5 | 0.35 | 0.04 | ||||
| 18 | C. manchuriensis | 4 | 0.29 | 0.03 | ||||
| 19 | C. lupicaris | 3 | 0.2 | 0.02 | ||||
| 20 | C. fasciipennis | 3 | 0.21 | 0.02 | ||||
| 21 | C. fasciipennis | 3 | 0.21 | 0.02 | ||||
| 22 | C. simulator | 2 | 0.14 | 0.01 | ||||
| 23 | C. pictipennis | 2 | 0.14 | 0.01 | ||||
| 24 | C. odiatus | 1 | 0.07 | 0.01 | ||||
| 25 | C. riouxi | 1 | 0.07 | 0.01 | ||||
| Total outdoor | 13,631 | 973.6 | 100 |
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_b | Tmax | Taver | Tmin | |
|---|---|---|---|---|
| 2012 | Correlation coefficient | 0.556* | 0.535* | 0.556* |
| Sig. (2-tailed) | 0.037 | 0.046 | 0.037 | |
| 2013 | Correlation coefficient | 0.718** | 0.769** | 0.658** |
| Sig. (2-tailed) | 0.01 | 0.000 | 0.002 | |
| 2014 | Correlation coefficient | 0.398* | 0.508* | 0.575** |
| Sig. (2-tailed) | 0.048 | 0.012 | 0.004 |
Kendall's correlation coefficients of dependencies between the Culicoides activity in 2012, 2013 and 2014, and the humidity, wind speed and rainfall
| Kendalls tau_b | Humidity | Wind speed | Rainfall | |
|---|---|---|---|---|
| 2012 | Correlation coefficient | -0.423 | -0.210 | 0.340 |
| Sig. (2-tailed) | 0.116 | 0.451 | 0.225 | |
| 2013 | Correlation coefficient | 0.116 | -0.207 | 0.071 |
| Sig. (2-tailed) | 0.582 | 0.347 | 0.768 | |
| 2014 | Correlation coefficient | -0.155 | 0.151 | -0.105 |
| Sig. (2-tailed) | 0.443 | 0.468 | 0.644 |

Scatter charts showing correlation between Culicoides numbers collected outdoors and temperature

Scatter chart showing no significant correlation between the Culicoides numbers collected outdoors and humidity, wind speed, or rainfall
© 2016 W. Stefański Institute of Parasitology, PAS
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