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

Adela Sarvašová; Alica Kočišová; Erika Liptáková; Helena Hiavatá; Bruno Mathieu

doi:10.1515/ap-2016-0103

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

, Alica Kočišová

, Erika Liptáková

, Helena Hiavatá

and Bruno Mathieu

From the journal Acta Parasitologica

https://doi.org/10.1515/ap-2016-0103

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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.

Keywords: Culicoides; indoor; outdoor; seasonal activity; Slovakia; Bluetongue virus

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.

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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

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

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

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

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

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

Table SIV a

Kendall's correlation coefficients of dependencies between the Culicoides activity in 2012, 2013 and 2014, and the maximum (T_max), mean (T_avar) and minimum (T_min) temperatures

Kendalls tau_b		T_max	T_aver	T_min
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

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_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