EXTERNAL SCIENTIFIC REPORT

Transcription

1 EXTERNAL SCIENTIFIC REPORT APPROVED: 8 February 2017 doi: /sp.efsa.2017.en-1182 A first estimation of Culicoides imicola and Culicoides obsoletus/culicoides scoticus seasonality and abundance in Europe Versteirt V 1, Balenghien T 2, Tack W 1 and Wint W 3 1 Avia-GIS NV, Zoersel, Belgium 2 Institut Agronomique et Vétérinaire Hassan II, Madinat Al Irfane, Rabat, Morocco 3 Environmental Research Group Oxford, Oxford, The United Kingdom Abstract Culicoides imicola and C. obsoletus/c. scoticus are considered important vectors in Europe for the transmission of bluetongue and Schmallenberg virus. The seasonality and abundance of C. imicola and C. obsoletus/c. scoticus was assessed in Europe based on literature, expert input and modelling techniques detecting the onset and end of the vector season. Culicoides obsoletus/c. scoticus has a large distribution across Europe and can often be found in high abundances. The abundance peak is driven by temperature and humidity and is reached late spring/early summer and fall. The species is sometimes found as adult overwintering in stables but numbers are rather low; this can however have implications for the overwintering of the bluetongue virus. Culicoides imicola is restricted to countries around the Mediterranean basin and the predicted abundance is lower and the species appears only later in spring with a peak in fall. European Food Safety Authority, 2017 Key words: Culicoides imicola, Obsoletus complex, seasonality, abundance models Question number: EFSA-Q Correspondence: ahaw@efsa.europa.eu EFSA Supporting publication 2017:EN- 1182

2 Disclaimer: The present document has been produced and adopted by the bodies identified above as authors. This task has been carried out exclusively by the authors in the context of a contract between the European Food Safety Authority and the authors, awarded following a tender procedure. The present document is published complying with the transparency principle to which the Authority is subject. It may not be considered as an output adopted by the Authority. The European Food Safety Authority reserves its rights, view and position as regards the issues addressed and the conclusions reached in the present document, Suggested citation: Versteirt V, Balenghien T, Tack W and Wint W, A first estimation of Culicoides imicola and Culicoides obsoletus/culicoides scoticus seasonality and abundance in Europe. EFSA supporting publication 2017:EN pp. doi: /sp.efsa.2017.en-1182 ISSN: European Food Safety Authority, 2017 Reproduction is authorised provided the source is acknowledged. 2 EFSA Supporting publication 2017:EN-1182

3 Summary The recent and recurrent outbreaks of vector-borne diseases of animal health concern (such as bluetongue and Schmallenberg disease) in Europe has underlined the need for a better understanding of the distribution, taxonomy and ecology of Culicoides spp. National surveillance campaigns were initiated across Europe and indicated that species of the Culicoides obsoletus/c. scoticus assemblage are the most widely distributed livestock-associated species in the temperate climate in Central Europe, whilst C. imicola remains to be a primary vector in countries around the Mediterranean Basin. We therefore considered these two species (or assemblages) in this study. To assess the risk for transmission it is not only important to know the distribution of the species, but also to gather information on (seasonal) abundance as well as start and end of the season. As a first step, distribution data of the national surveillance campaigns is currently being collected (often also identified to species level) and validated within VectorNet. In addition, the seasonal abundance and start and end of the season was investigated. Modelling the peak of abundance can only be done with detailed monthly data and collected in a standardised manner in several countries in Europe which is either difficult to obtain or not available for a whole season. We therefore opted to look for published information on seasonal abundance data across Europe, and to produce models only for the start and end of the season. From literature, data was extracted for 15 countries. Also, recent (unpublished) models predicting the abundance of C. imicola and C. obsoletus/c. scoticus in Europe were included in this report. The abundance models predict in general lower mean numbers for C. imicola than for C. obsoletus/c. scoticus. Based on the obtained literature and models, the season for C. imicola is predicted to start between week 1 and week 23, whilst the season ends between week 40 and week 52. For C. obsoletus/c. scoticus the season is assessed to start between week 1 to week 25 and ends between week 41 to week 52. The produced models will benefit when more information will become available, but can together with the literature data be used as baseline. Regional differences occur and need to be considered. 3 EFSA Supporting publication 2017:EN- 1182

4 Table of contents Abstract... 1 Summary... 3 Table of contents Introduction Background and Terms of Reference as provided by the requestor Additional information Data and methodologies Results Abundance modelling Culicoides imicola Culicoides obsoletus/c. scoticus Seasonality (start and end of season) Culicoides imicola Culicoides obsoletus/c. scoticus Seasonality across Europe Western Europe Northern Europe Southern Europe Eastern Europe Conclusions Recommendations References EFSA Supporting publication 2017:EN- 1182

5 1. Introduction 1.1. Background and Terms of Reference as provided by the requestor This contract was awarded by EFSA to: Contractor: Agro-Veterinary Information and Analysis (Avia-GIS) Contract: OC.EFSA.AHAW fwc1 Specific Contract Additional information Culicoides is a genus of biting midges (Ceratopogonidae) comprising almost 1,400 species worldwide. Many of them are known vectors of various animal health related diseases. In Europe, Culicoidesborne viruses emerged over the last decades causing economic damaging outbreaks of bluetongue (BT) or Schmallenberg disease. For a long time, Culicoides imicola was considered the main vector of BT virus in the Palearctic region. However, several other Culicoides species do play a role in transmission especially those belonging to the Avaritia subgenus (Diptera: Ceratopogonidae). The latter have been indicated as primary BT virus vectors in many European countries and their possible involvement in the maintenance and overwintering of BT virus has been suggested, even in regions where C. imicola Keiffer is present (De Liberato et al. 2011). In some cooler and wetter areas of southern Europe around the northern range margins of C. imicola (European Turkey, southern and eastern Spain, and southern France), these Palaearctic complexes may play a major role in transmission, either alongside or in the absence of C. imicola (Purse et al. 2008). The existing terms to describe the taxonomy of the Avaritia subgenus are various. Several authors use the term Obsoletus group to refer to some species of the Avaritia subgenus, namely C. obsoletus, C. scoticus, C. dewulfi and C. chiopterus, for which females are relatively morphologically close. Moreover, they use the term Obsoletus complex to refer to species for which it is not possible to reliably distinguish females by morphology, namely at least C. obsoletus, C. scoticus and C. montanus. On the other hand, the terms Obsoletus complex or Obsoletus group may be used, depending on the publications, to refer to different species assemblages. However, phylogenetic studies show that these assemblages are not phylogenetically consistent, and that the taxon C. obsoletus highlights an important cryptic diversity. The terms should then not be used anymore. But we reproduced in this document the terms used by the authors of the literature review. The seasonality of a species is defined as the fluctuation of the population over a season, e.g. the period in which the population starts to develop, reaches its peak abundance and starts to decline. This may slightly fluctuate from year to year and is influenced by several environmental factors. In temperate regions, such as Europe, the seasonal occurrence and abundance are key factors in arboviral outbreaks and vary widely depending on the regions (Mellor et al. 2000). The seasonal vector free period (SVFP) is defined as the period during which the risk on arboviral transmission is very low when captures of Culicoides species are below a maximum threshold. In the absence of sound evidence supporting the determination of the maximum threshold, total absence of C. imicola specimens and less than five parous Culicoides per trap is used (European Commission 2007). A study of C. obsoletus in England indicated that, although number of insects fluctuated markedly throughout the year, survival and blood-feeding rate varied much less over the season (Birley and Boorman 1982). In Northern Europe, most Culicoides species overwinter in the fourth larval stage and although live adult specimen can be found in stables during winter, their numbers seems to be insufficient to drive BTV outbreaks (Searle et al. 2014). In Southern Europe, Culicoides, as a group, are probably active throughout the year in some warm winter areas. In Sardinia, Foxi et al. (2014) found that when the number of Culicoides imicola declined, the number of Culicoides obsoletus complex was sufficiently high to allow transmission. In some (especially southern) regions, it is very difficult or even impossible to determine a SVFP. Environmental parameters such as mean 5 EFSA Supporting publication 2017:EN- 1182

6 temperature and humidity are known to influence the seasonal dynamics of insects and can therefore be used in models predicting their occurrence and abundance (Searle et al. 2012). For more temperate species, Baldet et al. (2008) did not observe any activity outdoors when the maximum temperature fell below 10.8 C and the minimum temperature below 5.8 C. Purse et al. (2011) and Scolamacchia et al. (2014) found that the best performing models based on a single set of predictors were climate models, followed by landscape and then host models. The main climatic factors that influence distribution, abundance and seasonality of Culicoides spp. are indeed temperature and precipitation (Purse et al. 2007, Purse et al. 2015). However, altitude and the soil type could also play a role in the distribution of the species (e.g. Culicoides spp. prefer enriched soils). At the more local farm level, the interplay between climatic and environmental variables (including temperature, relative humidity, light intensity, wind speed and the like) is complex, with changes in optimality from one species to the next and thus will influence the species dynamics. In laboratory circumstances (at a non-fluctuating temperature), larval development of C. imicola takes days at 20 C, 9-12 days at 25 C and 7-9 days at 28 C; egg and pupal development take between 1-5 days depending on the temperature but do not fluctuate much (Veronesi et al. 2009). In general, larval development takes days in summer and can be extended over winter in the final batch, whilst egg and pupal stage development take about 3-10 days. For two species, Culicoides imicola and Culicoides obsoletus/c. scoticus, literature was screened to detect possible seasonal abundance patterns and recent (unpublished) models predicting the abundance of both species in Europe are discussed. In addition, models predicting the start and end of their activity were constructed based on published environmental criteria. 6 EFSA Supporting publication 2017:EN- 1182

7 2. Data and methodologies To model the abundance of a species, a statistical relationship between known abundance values and the values of a series of selected predictor covariates must be made initially. These relationships are calculated for a set of sample locations, and the estimated equations then applied to maps of the covariates which provide values at a pixel resolution. This results in spatially explicit predictions of abundance. In this report, we discuss several abundance models that were created on the European scale for Culicoides imicola and Culicoides obsoletus/c. scoticus. To assess the start and end of the season, screening of the available literature on Culicoides imicola and/or Culicoides obsoletus/c. scoticus seasonality was done along with expert consultation to determine the important variables that could have an influence. The climatological data (MODIS) of 2015 was used to build the model. Along with the model, any information on seasonal dynamic patterns was extracted from the literature and reported. The start and end of the season were modelled based on threshold values that were extracted from literature. For C. imicola, the following variables were extracted: The species occurs only in regions with Rainfall: mm (although some found in areas with 1000mm rain) Annual Mean temperature: C (Purse et al 2007) Winter isotherm: 2 C Start of season is dependent on temperature Adult activity will start at 12 C /immature development will start around 10.5 C Maximum activity around C Optimal range for BTV transmission is between 15 and 25 C in Europe (Purse et al. 2015) End of season is dependent on temperature Lower than 8-10 C activity stops (Purse 2005) Lethal temperature = -4 C (Verhoef et al 2014) For C. obsoletus/c. scoticus, the following variables were extracted: The species occurs only in regions with Rainfall: >= 700mm Winter isotherm: -1.5 C Start of season is dependent on temperature Adult activity will start at 10 C End of activity: If temperature = 4 C for longer than 10 days (Goffredo et al. 2004) 7 EFSA Supporting publication 2017:EN- 1182

8 3. Results 3.1. Abundance modelling Culicoides imicola The abundance model for Culicoides imicola (Figure 1) was made using the model kindly provided by Dr. Kate Searle and Dr. Beth Purse (FP7 EDENext project; Searle et al. in prep.). As expected for an Afro-tropical species, C. imicola abundance is predicted to be low for Europe, except for Southern and Eastern European countries. The extent of C. imicola populations is over-predicted in SE Europe in the Balkans (e.g. Bulgaria, Macedonia, Hungary and Serbia where C. imicola is recorded to be absent by extensive vector surveillance), in N. Greece, S. France and N. Italy. The precise configuration of this species northern range edge is much better captured by the predicted habitat suitability map developed by Purse et al. (2007) that is congruent with vector surveillance data that have accumulated in the years since it was developed. We suggest that researchers wishing to use the abundance map in their models mask it by the predicted probability of presence from the Purse et al. (2007) model (Figure 2). Figure 1: Predicted logged peak summer abundance of Culicoides imicola across Europe from FP7 EDENext project (Searle et al. in prep.) averaged across the period from 2009 to EFSA Supporting publication 2017:EN- 1182

9 Figure 2: Predicted probability of presence of Culicoides imicola across Europe from environmental model developed by Purse et al Tatem et al. (2003) used Portuguese data from 87 sites surveyed in 2000 and 2001 to predict the possible abundance of Culicoides imicola in Europe and around the Mediterranean basin (Figure 3). In total, 41 variables were selected but only 7 were used for the abundance models. NDVI (Normalized Difference Vegetation Index) was the most important variable, high abundances were found in areas where NDVI peaked in mid-march. The model predicts some areas very well, but has its limitations and certainly has difficulties to predict areas in Eastern Europe. It is likely that the environmental determinants of C. imicola distribution in Eastern Europe were too different from those in Portugal that were used to build the model. However, the further inclusion of trap data from Eastern Europe would provide more confidence in the resultant prediction maps for this area. Withensaw et al. (2015) used weekly sampled data from sites in the UK and Spain to model the presence and abundance of C. imicola in Europe. The model predicts the distribution of C. imicola to be restricted to southern Europe (Figure 4), in line with previous prediction maps and sampled presence. However, there is under-prediction of presence in Spain and over-prediction in Italy and Bulgaria. 9 EFSA Supporting publication 2017:EN- 1182

10 Figure 3: Abundances of Culicoides imicola around the Mediterranean basin predicted by a model derived from the observed abundances at 87 sites in Portugal (Tatem et al. 2003). Figure 4: Abundances of Culicoides imicola based on data from the UK and Spain (Withensaw et al. 2015) EFSA Supporting publication 2017:EN- 1182

11 Culicoides obsoletus/c. scoticus The abundance model for Culicoides obsoletus/c. scoticus (Figure 5) was made using the national surveillance data of France, that was re-screened and for which more stringent quality filters were applied. Moreover, the results from survey locations in the UK, Iceland, Denmark, Norway, Finland and the most substantially from Portugal were used. The mean maximum annual abundance (as opposed to maximum annual abundance) was used as input for these models to remove extreme training set values. The model predicts a high mean abundance in large parts of Europe and countries around the Mediterranean Sea. Adding more information to the models could have an influence on the mean numbers but the trend would be comparable. Figure 5: Abundance model for Culicoides obsoletus/c. scoticus (Balenghien & Wint, unpublished work). The model of Whitenshaw et al. (2015) predicts higher abundance of what they consider as the C. obsoletus complex and C. pulicaris complex in northern Europe compared to the south (Figure 6) EFSA Supporting publication 2017:EN- 1182

12 Figure 6: Abundances of the Culicoides obsoletus complex, based on data from the United Kingdom and Spain (Withensaw et al. 2015) Seasonality (start and end of season) Culicoides imicola For Culicoides imicola, a suitability mask was generated excluding areas using two suitability constraints: annual precipitation between 300 and 700 mm and a mean January isotherm of 2 C. For these factors, binary masks were generated (1=suitable, 0=unsuitable), which were then combined to make a single suitability mask. Within the suitable areas, the start and end of the season was determined based on temperature on a weekly basis. The start of the season was defined by mean land surface temperatures (mean LST) exceeding 12 C; the end of the season was defined when mean LST was lower than 8 C. The start of the season (Figure 7) appeared to occur as early as week 1 and till week 23. The season came to an end at week 40 till week 52 (Figure 8) Culicoides obsoletus/c. scoticus For Culicoides obsoletus/c. scoticus, a suitability mask was created using the following constraints: annual precipitation >= 700 mm and a mean January isotherm of -1.5 C. The start of the season was defined by a mean LST exceeding 10 C and the end of the season by mean LST lower than 4 C. The start of the season (Figure 9) appeared to occur as early as week 1 and till week 25. The season came to an end at week 41 till week 52 (Figure 10) EFSA Supporting publication 2017:EN- 1182

13 Figure 7: Start of season (expressed as week number) for Culicodes imicola. Figure 8: End of season (expressed as week number) for Culicodes imicola EFSA Supporting publication 2017:EN- 1182

14 Figure 9: Start of season (expressed as week number) for Culicodes obsoletus/c. scoticus. Figure 10: End of season (expressed as week number) for Culicodes obsoletus/c. scoticus EFSA Supporting publication 2017:EN- 1182

15 3.3. Seasonality across Europe The literature obtained was screened on the presence of seasonal abundance data. Often the papers only contain data from one period and not an entire year as experts expect. Modelling abundances is still a less-used modelling technique and requires a special approach, particularly when abundance data is extracted from publications and reports as data is not comparable and it is difficult to draw conclusions from. In the ideal situation, monthly collection data should be available per Culicoides species, preferably for more than one year (to downscale year to year fluctuations) and, when modelling on a European scale, for several countries. This is not the case, many of the surveillance data is not freely available nor identified to the required level (only genus not species) and the collection efforts often differ from one country to the other. Adult Culicoides are mainly collected using UV-light/suction traps and more specifically by the model commercialized by the Onderstepoort veterinary institute (OVI) in South-Africa. This trap has been the most widespread trap used during national surveillance of the dynamics of Culicoides populations across Europe although exceptions exists. Abundance data obtained with other UV-light/suction traps (like the MiniCDC) could be reduced but these traps collect the same diversity than OVI traps. In some cases, Culicoides spp. were sampled using much less widespread traps such as the BGSentinel (Germany), the Rieb (France) and Pirbright (UK) traps. Venter et al. (2009) and del Rio et al. (2013) both concluded that the OVI and MiniCDC will collect higher numbers of Culicoide spp. compared to the above cited traps and therefore captures are comparable using a correction factor of x2.6 for MiniCDC Culicoides spp. abundance data (see Section 3.1). Besides the use of different traps, the trapping frequency (e.g. the number of collections) per month at one location differs and needs to be evened out. Table 1 shows the countries for which data was retrieved from the literature. Table 1: Overview of the countries and species for which data is collected. Culicoides obsoletus/c. scoticus Culicoides imicola Austria X Belgium X Czech Republic X France X X Germany X Great Britain X Greece X X Italy X X Portugal X X Romania X Slovakia X Spain X X Sweden X Switzerland X The Netherlands X 15 EFSA Supporting publication 2017:EN- 1182

16 Western Europe Austria (Brugger & Rubel 2013, Brugger et al. 2016) During this study a black light suction trap of Onderstepoort type was used. During the monitoring period (from January to December), a total of 18,952 Culicoides spp. was captured. The predominantly trapped complex was Obsoletus (85.7%), comprising C. obsoletus, C. scoticus, C. dewulfi, and C. chiopterus. The vector density varied temporally and spatially as a function of temperature and precipitation. The Obsoletus complex specimens were caught from May to November with a peak over summer, although other species were also found from early March till December. Basic reproduction numbers above one were generally found between June and August except in the mountainous regions of the Alps. Based on the data from C. obsoletus, they tried to predict the vector densities using a mathematical model (Figure 11). They conclude that it is remains difficult to estimate vector densities, even if numbers of trapped midges from a monitoring programme are available but that it could give a good indication for fine tuning surveillance. Figure 11: Daily (a), biweekly (b) and monthly (c) Culicoides obsoletus complex counts observed with the blacklight trap (bars) vs. predicted by the Poisson regression model (lines). Period Jan 2009 December 2010, Vienna Austria EFSA Supporting publication 2017:EN- 1182

17 Belgium (Fasotte et al. 2008, De Regge et al. 2015) Fassotte et al. (2008) describe a sampling done during 2006 where they compiled all captured Culicoides spp. Samples were taken at two different sites near Gembloux from 11 May to 31 December 2006 at site 1 and from 12 September to 13 October 2006 at site 2. Peak activity was observed in June with corresponded with an increase in temperature and decrease in precipitation compared to the preceding month (Figure 12). Low temperatures, heavy wind and rain are known to inhibit Culicoides spp. activity and are probably responsible for the low catches in October and November until the population died out due to the low temperatures in December. The final catch was at the beginning of December. Figure 12: Seasonal fluctuation of Culicoides spp. in two sites in Gembloux, Belgium (2008). De Regge et al. (2015) collected Culicoides (Diptera: Ceratopogonidae) in 2011 at 16 locations near stables covering four regions of Belgium with Onderstepoort Veterinary Institute (OVI) traps whilst at two locations Rothamsted suction traps (RSTs) were used. During January and February and July September, Culicoides were collected every second week, whereas during March June and October December, weekly catches were performed. Quantification of the collections and morphological identification showed important variations in abundance and species diversity between individual collection sites, even for sites located in the same region. Culicoides were present during most of the year with Culicoides obsoletus complex midges found from 9 February until 27 December (Figure 13). However, only one C. obsoletus complex species was found in February and it was not until the end of March that more were collected. The single catch in February can be linked to overwintering of adults in stables. Although the last catches occurred in December, the population starts rapidly declining from October-November. Highest numbers were observed over summer. The authors conducted a real-time reverse-transcription polymerase chain reaction to screen for Schmallenberg. They detected the virus first in August for the first time that year in specimens belonging to the C. obsoletus complex and detected again in September and October EFSA Supporting publication 2017:EN- 1182

18 Figure 13: Monthly spatiotemporal abundances of Culicoides in 2011 based on monitoring with 16 Onderstepoort Veterinary Institute (OVI) traps covering four regions of Belgium. Culicoides were monitored in Antwerp, Liège, Gembloux and Libramont with eight, five, one and two OVI traps, respectively. The mean number of Culicoides per collection is based on maximums of two (January, February, July, August, September), four (April, May, October, December) or five (March, June, November) collection dates in the respective month. France (Venail et al. 2012) From 2000 onwards, an intensive Culicoides trapping scheme was initiated in Corsica and in the Mediterranean littoral of French mainland (Figure 14). In Corsica, the two most abundant species, Culicoides imicola and C. obsoletus/c. scoticus, showed different seasonal dynamics. Culicoides imicola was present mainly from May to November, with highest abundance in August, September or October. Culicoides imicola populations progressively increased with monthly temperatures. Culicoides obsoletus/c. scoticus populations were abundant around May and declined during summer dry months. In Corsica, C. obsoletus/c. scoticus populations became usually rare in January however exceptions occur and in some years, C. obsoletus/c. scoticus can be found all year. Two species of the Obsoletus complex were dominant in mainland France, representing from 30 to 95% of the total annual catches. The species is present from March/April and declines in November. In generally C. imicola is abundant during summer in the littoral of Corsica and C. obsoletus/c. scoticus occurred widely and abundantly from spring to autumn on sheep and cattle holdings across the whole French mainland EFSA Supporting publication 2017:EN- 1182

19 Figure 14: Seasonal dynamics of Culicoides imicola and Culicoides obsoletus/c. scoticus in Corsica and of Culicoides obsoletus/c. scoticus in mainland France. Germany (Hoffman et al. 2009) Biting midges were captured with 89 black light traps (modified BG Sentinel) on farms in Germany during 7 consecutive nights in the first week of each month during the study period (April 2007 May 2008) (Figure 15). Most traps (n=85) were placed near cow sheds, either adjacent to barns or in their entrance area. The overall number of biting midges caught started at a moderate level (11,577) in April 2007, peaked in October (246,882), decreased to low levels during December 2007 March 2008, and started to rise again (462) in April Small numbers (66 81) of Culicoides spp. were also detected in some traps during January March The fact that so many Culicoides specimens were collected also over winter period, can be due to overwintering of adults in these animal sheds EFSA Supporting publication 2017:EN- 1182

20 Figure 15: Monthly catches of midges of the Obsoletus group (black), Pulicaris group (red), and other Culicoides spp. (blue). The Netherlands (Meiswinkel et al. 2013, Takken et al. 2008). Takken et al. (2008) studied different habitats in 2006 and collected 15 different species of which Culicoides obsoletus was the most abundant. In 2006, Culicoides spp. became active in all habitats only by the end of April. Continuous monitoring since 1 March 2006 revealed that the earliest date that Culicoides spp. were found on the farms was early May. Most the species were more abundant between May and mid-june compared to the consecutive period mid-june to end of July. Many Culicoides species were found until late in the phenological season and their activity was strongly associated with climate throughout the year. High annual variations in population dynamics were observed within the same study areas, which were probably caused by annual variations in environmental conditions. Below a figure of the catches at the livestock farms in the survey (Figure 16); catches are shown in a logarithmic scale. For C. obsoletus two clear peaks can be observed, one in summer and one in fall. Activity of the species started in 2006 in April. Meiswinkel et al. (2013) (Figure 17) conducted a survey during which sites were monitored in 2007 and In light trap collections were made; in collections were made. Culicoides spp. were captured using the Onderstepoort-type trap. The midge season in 2008 began approximately 2 3 weeks later than in 2007 and ended also sooner, shortening the 2008 midge year by approximately 1 month. During the bridging winter of 2006 and 2007 low levels of activity in the Obsoletus Complex occurred during six of the first 12 weeks of The activity of the Obsoletus Complex started in April and lasted until the end of November (a low number of specimens were still collected in the first weeks of December), at least two peaks were observed, one in June and one in August, but the activity remains high over summer-early fall EFSA Supporting publication 2017:EN- 1182

21 Figure 16: Livestock farms: log catches of 3 most abundant Culicoides species in Figure 17: (A) January to December 2007: average weekly biting midge abundances (n +1) on 21 cattle holdings in the Netherlands plotted on a log10 scale for 5 proven or potential bluetongue vector Culicoides species combined (C. chiopterus, C. dewulfi, C. obsoletus, C. scoticus and C. pulicaris; solid dark green line) compared with that for all Culicoides spp. (40 species; solid blue line). The dotted red line depicts the weekly mean of the daily temperature ( C). (B) January to December 2007: average weekly biting midge abundances (n +1) on 21 cattle holdings in the Netherlands plotted separately on a log10 scale for each of the proven or potential vectors for bluetongue virus i.e. the Obsoletus complex (C. obsoletus/c. scoticus) (solid pink line), C. dewulfi (solid light green line), C. chiopterus (solid light blue line) and C. pulicaris (solid orange line). The dotteded line depicts the weekly mean of the daily temperature ( C) EFSA Supporting publication 2017:EN- 1182

22 Switzerland (Kaufmann et al. 2012) Biting midges were caught on farms using the Onderstepoort blacklight suction traps operated once per week, from approximately 2 h before dusk and until after dawn. The campaign was carried out from June 2008 to May 2011 with a total 156 weeks (Figure 18). Significant activity (more than 10 midges per trap and night) was observed between April and November, and on average less than one midge was collected during the winter months (December to March) except for one location where a low abundance of around 10 midges were observed during the second and third year. It seems that in Switzerland the vector-free period (all species combined) lasts from week to week 12 14, depending on weather conditions. Figure 18: Data from the locations with high overall sampling reliability, i.e. at least 145 of the maximal 156 weekly catches available: A) Commugny (altitude 20 m) B) denswil ( 20 m) C) hlethurnen ( 70 m) D) Chateau d Oex (9 0 m) E) Chaumont (1,110 m) F) Juf (2,130 m). The monthly averages of total number of collected Culicoides biting midges (logarithmic scale) are shown by black (season 2008/2009), open (2009/2010) and grey (2010/2011) circles EFSA Supporting publication 2017:EN- 1182

23 Northern Europe Great Britain (Sanders et al. 2011) In 2008, a study was done in 12 sites; samples were collected once every 24 h from 31 March to 16 November using Rothamsted suction traps. A total of Culicoides spp. specimens were identified from the 2008 samples providing an estimated total catch of Culicoides spp. specimens over the 12 sites. Trap catches were dominated by the C. obsoletus group (48% of the total catch) and C. pulicaris C. punctatus (44%) species groups. A weekly summary of the numbers of Culicoides spp. specimens collected is given in Figure 19. The first collection of >5 specimens occurred mid-april 2008 and the population starts to decline in November. Figure 19: Seasonal fluctuation of Culicoides spp. in different sites across Europe. Seasonal trends with bimodal peaks (in spring and autumn) were identified for total Culicoides spp. and Obsoletus group females. By contrast, males of the Obsoletus group exhibited only a single underlying peak in abundance. The date of first collection of five or more Culicoides spp. specimens at each site was remarkably similar considering the differences in habitat and latitude between sites, but was influenced by the abundance of C. punctatus and C. pulicaris at some sites, which emerged earlier than members of the Obsoletus group. C. obsoletus group showed a peak in summer. Sweden 23 EFSA Supporting publication 2017:EN- 1182

24 To determine the diversity, distribution and seasonal dynamics of Culicoides spp., weekly collections were made during 2008 and during March-December 2009 using the Onderstepoort Veterinary Institute black light trap. Twenty sampling sites were selected in 12 provinces. In total, 30,704 Culicoides were collected in 2008 and 32,252 in The most abundant species were the potential vectors of BTV Culicoides obsoletus/scoticus that comprised of 77% of the total catches and they occurred as far north as latitude 65 N. Culicoides obsoletus/scoticus were most abundant during May- June and August-September. However, most species were active from March to November in 2008 and April to October in Southern Europe Greece (Patakakis et al. 2009) The authors divided mainland Greece into 59 squares measuring 50 x 50 km that were sampled for Culicoides spp. between 1999 and 2004 using Onderstepoort suction traps (OVI). Wherever possible, two farms at least 10 km apart were sampled in each quadrant. Each farm was sampled overnight on two occasions between the months of April and November. Farms where C. imicola was found during this period were sampled for a further two or three nights during the winter months (December- March). The activity of biting midges seems to last until the end of December and start again around mid-march depending on the weather conditions (Figure 20). Figure 20: Seasonal presence/absence of Culicoides imicola, Obsoletus and Pulicaris- groups at Nea Santa (northern mainland), Omolio (central mainland) and Dimila (Rhodes) EFSA Supporting publication 2017:EN- 1182

25 Italy (De Liberato et al. 2010, Goffredo et al. 2013, Foxi et al. 2016) Between 17 January 2002 and 31 December 2005, 3,944 light trap (OVI) collections were carried out in 189 trap sites, distributed in all the 15 provinces of Lazio and Tuscany (De Liberato et al. 2010). Culicoides obsoletus group was recorded in 181 out of 189 trap sites (95.8%). Figure 21: Overall mean monthly collection of C. obsoletus group per trap night calculated across all trap sites in the study area. Figure 22: Temporal trend of C. obsoletus group abundance along the period January 2002 through December Median, 25th and 75th percentiles, range and outliers are represented. Goffredo et al collected Culicoides spp. at six sites between June 2011 and June A total of 33,724 Culicoides were sampled. Species belonging to the Obsoletus Complex were the most abundant (94.44%) and, within the complex, Culicoides obsoletus was the most prevalent species in 25 EFSA Supporting publication 2017:EN- 1182

26 the studying area (65.4%). No Culicoides were present in the collections made between November 15th 2011 and March 22nd 2012, where after the vector population slowly started to increase. No indication was given on the peak of abundance Foxi et al. (2016) studied different Culicoides spp. in Sardinia using light traps on a number of selected farms. Trapping was carried out during once a week in 2001, 2003 or Culicoides imicola was never or rarely captured during the first five months of the year, which was followed by a rapid population increase starting from July and reaching the peak in summer-autumn (Sassari-2, 2008). In the southern farm, an earlier population growth was recorded in April. The number of parous females represented 45 % of total females. Culicoides scoticus was detected during the whole year with 3 4 population peaks depending on the farm, and was generally more abundant during the first or the last months of the year. Similarly, C. obsoletus was detected over the whole year, but the highest density was recorded during summer. Spain (Ortega et al. 1998, Perez et al. 2012, Romon et al. 2012) Ortega et al. (1998) conducted a survey of fifteen sites in twelve provinces of central Spain and Andalusia using Pirbright traps. A total of 293,625 Culicoides specimens were collected in 1387 samples over a two-year period. These comprised approximately 9.2% Culicoides imicola, 11.4% Pulicaris group, 1.6% Obsoletus group and 12.2% C. circumscriptus. Culicoides imicola was present at ten of the fifteen sites; the five sites from which it was absent were the most eastern of the fifteen. Pulicaris group were present at all sites; Obsoletus group were present at twelve sites. The annual peaks in abundance were: C. imicola, August-October; Obsoletus group, May-June; and Pulicaris group, March-June. Perez et al. (2012) conducted a similar research in Andalusia during using minicdc traps located on 56 cattle farms distributed throughout the eight provinces of Andalusia. From January 2007 to December 2008, traps were activated and samples collected weekly. 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 = 8,190). Captures were seasonal and mostly occurred in May November. Culicoides associated with livestock were captured using CDC blacklight traps at three BTV-infected farms in Basque Country between November 2007 and December Few specimens of C. imicola were captured, Culicoides obsoletus/c. scoticus (two sibling species of the Obsoletus complex) were dominant throughout all months and sexes with maximum phenological peaks in November 2007 and June July Culicoides obsoletus/c. scoticus parous minimum infection rates were 0.01 in November December, in January February and nil in March. Miranda et al. (2004) captured midges on four cattle farms in Majorca and on three in Minorca, during one night per week from June 2001 to December 2002 (Figure 23 and Figure 24). The traps were operated from one hour before sunset to one hour after sunrise. Results showed that Culicoides imicola is the predominant species on Majorca, but its numbers did not differ significantly from those of C. obsoletus. Important differences were found between the abundances of C. imicola and C. obsoletus on Majorca and Minorca which is probably due to different farming practices or differing environmental conditions. The results from 2001 and 2002 indicate that the seasonal abundance of C. imicola was highest during September and October, whereas C. obsoletus showed a period of peak abundance between April and July EFSA Supporting publication 2017:EN- 1182

27 Figure 23: Seasonal fluctuation of Culicoides imicola, C. obsoletus and Culicoides spp. adult populations on the island of Majorca, Spain. Figure 24: Seasonal fluctuation of Culicoides imicola, C. obsoletus and Culicoides spp. adult populations on the island of Minorca, Spain EFSA Supporting publication 2017:EN- 1182

28 Portugal (Ribeira et al. 2014) Mainland Portugal was divided into 45 geographical units (GUs) each 50 x 50 km, within each GU, farms located at a minimum distance of 10km from other sampled holdings and at least 2.5km from the coast, containing a minimum of five horses or ruminants, were identified. A CDC light trap was operated from dusk and deactivated it at dawn from September 2005 and December The number of collections by month varied from a minimum of 37 catches (0.65% of total) in December 2010 to 135 catches (2.4% of total) in April The months with the highest number of catches were April 2008, March 2009, March 2007 and July Regarding the season of the year, the highest number of catches occurred during autumn (1,587 catches, 28% of total) while the lowest number of catches was verified in winter (1,186 catches, 21% of total). Figure 25: Seasonality of Culicoides imicola and Obsoletus group between September 2005 and November In general, C. imicola activity began between March and April, but between 2007 and 2008 there were collections of a limited number of specimens in January. The largest collections of this species were made in July, August and September 2006 and September and October 2007, with collections exceeding 100,000 specimens. In the centre of the country peak activity was observed between September and October, while in the southern regions the period of highest activity of C. imicola extended between September and November. Although in small numbers, seasonal activity of Obsoletus group was detected as early as January. In the northern region, this species reached the highest abundances between May and August, while in the central regions this occurred between May and June. In the southern regions, Obsoletus group typically reached peak abundance between April to May. The abundances of C. imicola and the Obsoletus group were lowest during winter (December-January-February). This was more pronounced for C. imicola, however, in both cases a proportion of the females collected during winter were parous, ranging from 20.3% (in 2006) to 76.4% (in 2009) for C. imicola and from 13.3% (2005) to 35.3% (2007) for the Obsoletus group EFSA Supporting publication 2017:EN- 1182

29 Eastern Europe Czech Republic (Radrova et al. 2015) An extensive survey was done between 2008 and 2013 at 34 sampling sites using CDC black-light suction traps that were placed overnight near ruminants in farms or in forest game preserves. The Culicoides obsoletus species group, incriminated as a bluetongue virus vector, was predominant in both domestic livestock (91%) and semi wild game (52%). A relatively high proportion (around 30%) of C. obsoletus Meigen females with pigmented abdomen was observed from spring till autumn. Numbers of C. obsoletus were highest during the spring, but several peaks appeared during the seasons. In all analyzed years, numbers of C. obsoletus significantly decreased in late October and the latest specimens were captured on November 27, 2009 and December 2, The earliest capture of C. obsoletus was on March 25, In , traps ran continuously during the whole winter at the four selected cattle farms, but no Culicoides were found in winter months. Romania (Oprescu et al. 2008) The study done from May to September 2005 (with 6 collections per month) using lightened movable traps (trap type not specified). In total, for the 30 nights of study, 4159 Culicoides spp. were collected, of which 2384 were Culicoides obsoletus complex. The authors found that for two complexes Culicoides obsoletus complex and C. pulicaris complex, the number of collected individuals was directly correlated with the mean temperature. The number of specimens caught in May and June did not differ much, most specimen were found in July whilst in August-September the population decreased. Slovakia (Sarvasova et al. 2016) Although the study did not intend to capture the seasonality of the biting midges rather than to investigate the difference between species captured in and outside stables; it shows a similar trend: in each studied year, activity of Culicoides spp. peaked at mid-june and remained high during summer months (Figure 26). It also shows that there is a correlation between Culicoides spp. abundance and temperature. Only when the temperature remains high enough in October, the number of biting midges caught remain high, otherwise a decrease of the population was observed. A higher Culicoides spp. activity outdoors during the summer, compared to the highest indoor activity in autumn was observed. Weekly variations in overall densities (per trap per night) of Culicoides spp. caught outdoors and indoors were found to be related to outdoor temperatures. The main species collected both in- and outdoors were Culicoides obsoletus/scoticus and Culicoides punctatus EFSA Supporting publication 2017:EN- 1182

30 Figure 26: Seasonal occurrence of Culicoides spp. in Slovakia EFSA Supporting publication 2017:EN- 1182

31 4. Conclusions Assessing the seasonal population dynamics is an important factor in a wide range of fields such as establishing disease risk estimations, implementing surveillance and protection/control measures. Based on literature review, it was confirmed that seasonality of both Culicoides imicola and Culicoides obsoletus/culicoides scoticus was driven by temperature and humidity. Winter usually stops the activity of C. obsoletus/c. scoticus, except in some areas of the Mediterranean basin or of the Atlantic coast, where mid temperatures of some years may lead to continuous activity through the year. Active populations appear from February (under oceanic climate) to May (under continental climate) in Europe, depending of spring temperatures. The peak of abundance occurs from May to July depending on spring temperatures and summer dryness. In most areas (Mediterranean or continental climates), populations decrease during summer due to summer dryness, before highlight a second peak of abundance in autumn after rainfalls, whereas under oceanic climates, populations may be maintained at high level during the summer. Population abundance decreases in October or November and then disappears. The disappearance timing is determined by the precocity of winter temperatures. Some adults could be found during winter even in Northern Europe. In Northern Europe, the large majority of them are nulliparous females. This could be the consequence of recent emergences due to transitory increases of temperatures during winter. Table 2: Overview of the start (>5 females) and end of the season with the period indicating the peak of abundance. Culicoides obsoletus/c. scoticus Start End Peak Austria May November July-August (summer) Belgium May November July-August (summer) Czech Republic April November Different peaks England April November Unclear (probably over summer) France March/April November Different peaks Germany April November Unclear (probably over summer) Greece February December - Italy April (southern: January) November/ December June-July Portugal May December Summer (July-August) Romania May September Different peak Slovakia Peak over summer (decline after September) Spain Dependent on region Summer, fall (two peaks) Sweden March/April October/November 2 peaks (May/June and August/September) Switzerland April November Summer The Netherlands April November Summer For Culicoides imicola, the main driver is again the temperature, but humidity and NDVI also play a role. Collections of individuals are usually rare during spring. Populations appear in early summer and increase progressively to reach a peak of abundance in late September, October or early November. Then populations decrease often below 10, and in some regions of south Europe captures could be null during winter EFSA Supporting publication 2017:EN- 1182