Skip to main content
Download PDF

Abundance and diversity of Culicoides Latreille (Diptera: Ceratopogonidae) in southern Ontario, Canada

Parasites & Vectors volume 16, Article number: 201 (2023) Cite this article

Abstract

Background

Culicoides Latreille (Diptera: Ceratopogonidae) is a genus of hematophagous midges feeding on various vertebrate hosts and serving as a vector for numerous pathogens important to livestock and wildlife health. North American pathogens include bluetongue (BT) and epizootic hemorrhagic disease (EHD) viruses. Little is known about Culicoides spp. distribution and abundance and species composition in Ontario, Canada, despite bordering numerous U.S. states with documented Culicoides spp. and BT and EHD virus activity. We sought to characterize Culicoides spp. distribution and abundance and to investigate whether select meteorological and ecological risk factors influenced the abundance of Culicoides biguttatus, C. stellifer, and the subgenus Avaritia trapped throughout southern Ontario.

Methods

From June to October of 2017 to 2018, CDC-type LED light suction traps were placed on twelve livestock-associated sites across southern Ontario. Culicoides spp. collected were morphologically identified to the species level when possible. Associations were examined using negative binomial regression among C. biguttatus, C. stellifer, and subgenus Avaritia abundance, and select factors: ambient temperature, rainfall, primary livestock species, latitude, and habitat type.

Results

In total, 33,905 Culicoides spp. midges were collected, encompassing 14 species from seven subgenera and one species group. Culicoides sonorensis was collected from three sites during both years. Within Ontario, the northern trapping locations had a pattern of seasonal peak abundance in August (2017) and July (2018), and the southern locations had abundance peaks in June for both years. Culicoides biguttatus, C. stellifer, and subgenus Avaritia were significantly more abundant if ovine was the primary livestock species at trapping sites (compared to bovine). Culicoides stellifer and subgenus Avaritia were significantly more abundant at mid- to high-temperature ranges on trap days (i.e., 17.3–20.2 and 20.3–31.0 °C compared to 9.5–17.2 °C). Additionally, subgenus Avaritia were significantly more abundant if rainfall 4 weeks prior was between 2.7 and 20.1 mm compared to 0.0 mm and if rainfall 8 weeks prior was between 0.1 and 2.1 mm compared to 0.0 mm.

Conclusions

Results from our study describe Culicoides spp. distribution in southern Ontario, the potential for spread and maintenance of EHD and BT viruses, and concurrent health risks to livestock and wildlife in southern Ontario in reference to certain meteorological and ecological risk factors. We identified that Culicoides spp. are diverse in this province, and appear to be distinctly distributed spatially and temporally. The livestock species present, temperature, and rainfall appear to have an impact on the abundance of C. biguttatus, C. stellifer, and subgenus Avaritia trapped. These findings could help inform targeted surveillance, control measures, and the development of management guides for Culicoides spp. and EHD and BT viruses in southern Ontario, Canada.

Graphical Abstract

Background

Culicoides Latreille (Diptera: Ceratopogonidae) is a genus of hematophagous flies, also known as biting midges, which feed on a variety of vertebrate host species [1,2,3]. This group includes > 1400 species worldwide that are on most major land masses across a variety of habitats, including agricultural and forested areas [1, 4, 5]. Some species of biting midges can contribute to poor performance in livestock from nuisance biting alone, and some also are competent vectors of zoonotic pathogens (e.g., Oropouche virus and Mansonella ozzardi) and important livestock and wildlife pathogens (e.g., Schmallenberg virus [SBV], African horse sickness virus, bluetongue virus [BTV], and epizootic hemorrhagic disease virus [EHDV]) [2, 6,7,8]. While in North America, two Culicoides spp., C. sonorensis and C. insignis, have been identified as capable of transmitting BTV and EHDV, a more complete understanding of vector competence for these viruses is lacking [9,10,11,12,13]. Other Culicoides species have been implicated as potential vectors as well (C. stellifer, C. paraensis, C. obsoletus, C. haematopotus, C. occidentalis, C. venustus) [14, 15].

These viruses pose a serious animal health threat, as BTV can cause high rates of mortality in domestic sheep [16], and both BTV and EHDV have the potential to cause high mortality among farmed and free-ranging cervids in North America, primarily white-tailed deer (Odocoileus virginianus) [17,18,19]. Recently, the frequency and geographic range of Culicoides spp.-driven virus outbreaks, specifically involving BTV, EHDV, and SBV, have increased in Europe, North America, and the Middle East, and have led to concerns about geographic spread [19,20,21,22,23]. Historically, epidemiologic patterns and the geographical distribution of both BTV and EHDV have been consistent [18]. However, the previously defined geographical limits of these viruses are changing, with outbreaks occurring more frequently and in areas not previously considered at risk [7, 19, 23, 24].

Long-standing changes in virus distribution may reflect a shifting geographic range of the vector largely in response to global climate change [19, 25]. For example, C. sonorensis (Wirth & Jones) has primarily been documented in portions of the western U.S. and Canada, with scattered populations east of the Mississippi River, but absent from the northeastern U.S. and eastern Canada, with C. sonorensis being recently recorded from a few regions of southern Ontario, Canada [7, 26,27,28,29,30]. While these new records are notable, Culicoides spp. community data are lacking from a broader region across southern Ontario and are needed to more accurately assess species diversity and abundance changes to past/current distribution. This information is crucial to determine the risk of Culicoides spp.-transmitted viral infections in domestic and wild ruminant populations in southern Ontario.

The emergence and re-emergence of pathogens transmitted by Culicoides spp. across North America, Europe, and the Middle East highlight the need for more intensive surveillance efforts that encompass vectors, viruses, and hosts. Few published studies have focused on characterizing Culicoides spp. composition and geographic distribution and the effects of potentially important, external factors that could contribute to species diversity and abundance [8, 19, 23]. This is especially true for areas such as Ontario, Canada, due to its northern latitude and the lack of reports of EHDV and BTV detection in livestock or wildlife prior to 2017 [23]. Therefore, the overarching goal of this study was to provide baseline data characterizing Culicoides spp. in sites that overlap with livestock and deer populations across southern Ontario, Canada. Specifically, our objectives were to (1) determine the relative abundance and taxonomic diversity of adult Culicoides spp. midges, and (2) assess the potential effects of meteorological and ecological variables on the abundance of documented Culicoides spp. (specifically those with highest abundance) across parts of southern Ontario, Canada.

Methods

Sample collection and identification

In 2017 and 2018, from June through October, insect surveys of southern Ontario farms were conducted and trap contents were processed as described previously [31]. Briefly, 11 farms, resulting in 12 survey sites (one farm moved between survey years), were classified as bovine (domestic cattle) or ovine (domestic sheep) primary sites (Fig. 1) and “northern” or “southern” sites. Farms consisted of primarily pastured animals. At each site, approximately every 2 weeks, two ultraviolet (UV) light-emitting diode (LED) Centers for Disease Control and Prevention (CDC) light traps (Model #2770, BioQuip Products Inc., Rancho Dominguez, CA, USA, http://www.bioquip.com) were deployed at recurring locations: within 15 m of outdoor livestock (deemed “livestock” habitat) and within 15 m of a natural area (deemed “natural” habitat, i.e., forested or wetland areas inaccessible to livestock). All collected insects were initially sorted at the University of Guelph (Guelph, Ontario), and Culicoides spp. were separated and shipped to the Canadian Food Inspection Agency (Lethbridge, Alberta) and the Southeastern Cooperative Wildlife Disease Study (Athens, GA) for morphological identification to species. Culicoides identified as members of the subgenus Avaritia were tallied and archived for future study.

Fig. 1
figure 1

Distribution of Culicoides spp. trapping sites based on farm type (ovine, bovine) in southern Ontario, Canada in 2017 and 2018, including trapping sites where Culicoides sonorensis was reported. Lines within landmass are based on Canadian census boundaries

Full size image

Peak abundance

Individual Culicoides spp. were sorted into groups based on their sex (male/female), species/subgenus, site, date, and trap location. The assessment of overall Culicoides spp., C. biguttatus, C. stellifer, and subgenus Avaritia peak abundance in 2017 and 2018 was standardized by use of an epidemiological week model (“epi-week”). This facilitates comparison of data across both years, as well as with datasets from other regions [32]. We defined the first epi-week of the year as the week that ended on the first Saturday in January with at least four preceding days in that month. Each epi-week began on Sunday and ended on Saturday. Therefore, in 2017, the first epi-week started on Sunday, January 1, and ended on Saturday, January 7. In 2018, the first epi-week began on Monday, January 1, and ended on Saturday, January 6.

Statistical analyses

Statistical analyses were performed for the individual species and/or species groupings with more than 1000 individuals, as well as those with potential involvement in orbivirus transmission [7, 15, 33, 34]. These included those within the subgenus Avaritia, as well as C. biguttatus and C. stellifer. To investigate independent variables affecting the nightly abundance of the subgenus Avaritia, C. biguttatus, and C. stellifer, mixed-effects univariable and multivariable negative binomial regression models were fitted to account for overdispersion in the data [35].

Nine independent variables were included in our univariable models: primary on-site livestock species (“ovine” vs. “bovine”), habitat type (“natural” vs. “livestock”), latitude (“northern” sites vs. “southern” sites), sum of rainfall (mm; for 2-day periods that encompassed the trapping period as well as 4 and 8 weeks prior to trapping), and mean temperature (°C; for the same time periods as rainfall). Data on mean daily temperature and total rainfall were acquired from Environment Canada [36] and represented the nearest or next-nearest weather station to each site (i.e., Sarnia, ON; Strathroy-Mullifarry, ON; Chatham Kent, ON; Kingsville Ministry of the Environment, ON; Markdale, ON; Kincardine ON) for corresponding sampling time periods in 2017 and 2018.

The linearity assumption for the continuous variables of sum of rainfall (in mm, for 2-day periods that encompassed the trapping period as well as 4 and 8 weeks prior to trapping), and mean temperature (in °C; for the same time periods as rainfall) were visually assessed via lowess (i.e., locally weighted scatterplot smoothing) curves. Based on the nonlinearity of the curves, the temperature and rainfall data were each categorized into three categories based on tertiles (Table 1). In addition, the correlations between independent variables were assessed using various correlation statistics depending on the form of the variables (e.g., phi coefficients and Spearman rank correlation coefficients). If the correlation exceeded |0.8|, only one of the variables would be considered for inclusion in a multivariable model based on biological plausibility. To account for potential clustering due to repeated sampling, we initially included residence (farm site), trap ID, and trap ID date as random intercepts.

Table 1 Results of mixed-effects univariable negative binomial regression examining the associations between environmental factors and the abundance of Culicoides stellifer, Culicoides biguttatus, and subgenus Avaritia for all trapping sites in southern Ontario, Canada in 2017 and 2018
Full size table

Multivariable models were fitted using a manual backward elimination process. Variables were retained in the models if they were statistically significant, based on a significance level of 5% (i.e., α = 0.05), or acted as an explanatory antecedent or distorter variable (i.e., a confounding variable). A variable was considered a confounding variable if it was a non-intervening variable and its removal from the model resulted in a greater than 30% change in the coefficient of a statistically significant variable. Random intercepts were removed from models if their variance component was very small (i.e., less than 1 × 10−5) and its removal did not impact the interpretation of the fixed effects in the model. The normality and homoscedasticity of the best linear unbiased predictions (BLUPs) were assessed graphically using normal quantile plots and examining a scatter plot of the BLUPs against the predicted outcomes, respectively. In addition, we examined Pearson residuals to identify outliers.

All statistical tests were performed using STATA (STATA Intercooled 14.2; StataCorp, College Station, TX, USA).

Results

Descriptive statistics

Throughout both 2017 and 2018 (resulted in 396 trap nights of collections), a total of 33,905 individual insects identified as adult Culicoides spp. were trapped, encompassing 14 species belonging to seven subgenera and one species group [31] (Fig. 2).

Fig. 2
figure 2

Distribution of Culicoides spp. in southern Ontario, Canada in 2017 and 2018. Pie charts show the percentages of adult Culicoides spp. trapped (including catch from each habitat type and both years). Culicoides spp. were included in the pie chart if ≥ 10 individuals had been trapped. This map includes the 11 farms, representing 12 sites. One site (asterisk) had a slight shift (6 km) in one location from 2017 to 2018, and was represented by one pie chart. Lines within landmass are based on Canadian census boundaries

Full size image

In 2017, 19,160 individual, adult Culicoides spp. were trapped; these represented 14 species from seven subgenera and one species group (Table 2). Those within the subgenus Avaritia (Fox) were the most abundant, followed by C. biguttatus (Coquillett) and C. stellifer (Coquillett), collectively accounting for 89.9% of the 2017 collection. Female Culicoides spp. (97.4%; n = 18,667) were more abundant than males (2.6%; n = 493), with a female-to-male sex ratio of 38:1. Culicoides spp. midges were more abundant in northern (71.8%; n = 13,756) versus southern trapping sites (39.3%; n = 5404) (Table 3). Among Culicoides spp. trapped in 2017, two subgenera and 10 species were collected from both northern and southern sites (Table 3). Additionally, midges were more abundant in the traps in livestock habitat (71.9%; n = 13,781) than in traps in natural habitat (28.1%; n = 5379) (Table 4). Culicoides sonorensis (0.1%; n = 14) females were trapped from two sites in 2017 (Fig. 1).

Table 2 Numbers of individual, adult Culicoides spp. trapped across all study sites in southern Ontario, Canada in 2017 and 2018
Full size table
Table 3 Numbers of individual, adult Culicoides spp. trapped in northern and southern site locations in southern Ontario, Canada in 2017 and 2018
Full size table
Table 4 Numbers of individual, adult Culicoides spp. trapped in livestock and natural habitats sites in southern Ontario, Canada in 2017 and 2018
Full size table

In 2018, we trapped a total of 14,745 individual, adult Culicoides spp. that represented 14 species from seven subgenera and one species group (Table 2). Culicoides biguttatus (Coquillett) was the most abundant species, followed by species within the subgenus Avaritia (Fox), and C. stellifer (Coquillett); these species accounted for 86.1% of the 2018 collection. Female Culicoides spp. (97.1%; n = 14,322) were more abundant than males (2.9%; n = 423), with a female-to-male sex ratio of 34:1. Culicoides spp. were more abundant in northern (55.3%; n = 8152) versus southern sites (44.7%; n = 6593) (Table 3). Three subgenera and eight species were collected from both northern and southern sites (Table 3). Additionally, Culicoides spp. were more abundant in livestock habitat (60.4%; n = 8904) than natural habitats (39.6%; n = 5841) (Table 4). Culicoides sonorensis (0.01%; n = 2) females were trapped at one site in 2018. Morphological identification to species of 270 specimens was precluded by post-collection artifacts and these were classified as Culicoides spp.

In 2017, adult Culicoides spp. peak abundance across the northern locations had multiple crests, including mid-July, mid-August, and late September [July 16–22 (epi-week 29); C. biguttatus, C. stellifer, and subgenus Avaritia), August 13–16 (epi-week 33); C. stellifer and subgenus Avaritia), and September 24–30 (epi-week 39); subgenus Avaritia] (Fig. 3). Across southern locations, there was a peak of abundance during mid-June [June 11–17 (epi-week 24); C. biguttatus]. In 2018, adult Culicoides spp. peak abundance in the northern locations had two activity peaks in mid-July and the end of July [July 8–14 (epi-week 28); C. biguttatus and subgenus Avaritia and July 22–28 (epi-week 30); C. stellifer]. For the southern locations, a peak of abundance occurred in mid-June [June 10–16 (epi-week 24); C. biguttatus] (Fig. 3).

Fig. 3
figure 3

Abundance of adult Culicoides spp. (all) (a), Culicoides biguttatus (b), subgenus Avaritia (c) and C. stellifer (d) by epi-week (Central Massachusetts Mosquito Control Project 2022) from northern and southern locations in southern Ontario, Canada (June–October 2017 and 2018). For southern locations in 2017, trapping occurred in epi-week 24, 26, 28, 29, 30, 31, 32, 34, 36, 38, 40; and for 2018: 24, 25, 27, 29, 31, 34, 35, 37, 41. For northern locations in 2017, trapping occurred in epi-week 25, 27, 29, 31, 33, 35, 37, 39, 41; and for 2018: 23, 26, 28, 30, 32, 34, 36, 38, 40

Full size image

Univariable mixed models

Overall, the temperature throughout the two study years ranged from 9.5 to 31.0 °C on trap days, 10.3–25.0 °C 4 weeks prior, and −5 to 25.0 °C 8 weeks prior (Table 1). Rainfall throughout the study ranged from 0.0 to 17.9 mm on trap days, 0.0–20.1 mm 4 weeks prior, and 0.0–72.0 mm 8 weeks prior (Table 1). Based on univariable analyses, C. stellifer was significantly more abundant at mid- to high-temperature ranges on trap days (i.e., 17.3–20.2 and 20.3–31.0 °C compared to 9.5–17.2 °C) and on sites with ovine as the primary livestock type compared to bovine (Table 1). Culicoides stellifer was significantly less abundant if the rainfall 4 weeks prior was between 0.1 and 2.6 mm compared to 0.0 mm and if insects were trapped in natural habitats compared to livestock habitats (Table 1). Culicoides biguttatus was significantly more abundant if temperatures on trap days were in mid to high ranges (i.e., 17.3–20.2 and 20.3–31.0 °C compared to 9.5–17.2 °C), if the rainfall 8 weeks prior was from 0.1 to 2.1 mm (compared to 0.0 mm) and with ovine as the primary livestock type (compared to bovine) (Table 1). Culicoides biguttatus was significantly less abundant if temperatures 4 weeks prior were higher (i.e., 21.1–25.0 °C compared to 10.3–17.3 °C), 8 weeks prior when 16.6–20.3 and 20.4–25.0 °C compared to −5.0 to 16.5 °C, and if rainfall 4 weeks prior was from 2.7 to 20.1 mm (compared to 0.0 mm) (Table 1). Subgenus Avaritia was significantly more abundant if the temperature on trap days was in mid- to high-temperature ranges (i.e., 17.3–20.2 and 20.3–31.0 °C compared to 9.5–17.2 °C), if rainfall 8 weeks prior was between 0.1 and 2.1 mm compared to 0.0 mm and at sites with ovine as the primary livestock type compared to bovine (Table 1). Subgenus Avaritia were significantly less abundant at natural habitats compared to livestock habitats and at southern sites compared to northern sites (Table 1).

Multivariable mixed models

Based on multivariable analysis, C. stellifer abundance was significantly greater on farms with ovine livestock compared to bovine, and with temperatures on trap days at 17.3–20.2 °C or 20.3–31.0 °C compared to 9.5–17.2 °C. Culicoides stellifer abundance was significantly lower if rainfall 4 weeks prior to trapping was between 0.1 and 2.6 mm compared to 0.0 mm and the temperature 8 weeks prior was 16.6–20.3 or 20.4–25.0 °C compared to −5.0 to 16.5 °C (Table 1).

The abundance of Culicoides biguttatus was significantly greater on farms with ovine livestock compared to bovine, and were significantly lower when temperature 4 weeks prior was 21.1–25.0 °C compared to 10.3–17.3 °C, rainfall 4 weeks prior was 0.1–2.6 mm compared to 0.0 mm, temperature 8 weeks prior was 16.6–20.3 °C or 20.4–25.0 °C compared to −5.0 to 16.5 °C, and rainfall 8 weeks prior was 2.2–72.0 mm compared to 0.0 mm (Table 1).

The abundance of subgenus Avaritia was significantly greater on farms with ovine livestock compared to bovine, with temperature on trap days at 17.3–20.2 °C or 20.3–31.0 °C compared to 9.5–17.2 °C, rainfall 4 weeks prior at 2.7–20.1 mm compared to 0.0 mm, and rainfall 8 weeks prior at 0.1–2.1 mm compared to 0.0 mm. The abundance of subgenus Avaritia was significantly lower with temperature 8 weeks prior at 20.4–25.0 °C compared to −5.0 to 16.5 °C, in natural habitat compared to livestock, and in farms located further south (Table 1).

The BLUPs for all models met the assumptions of normality and homoscedasticity. Potential outliers were identified, but their removal from the models did not change the interpretation of the models presented and no recording errors were identified.

Discussion

Although Culicoides spp. can be a severe nuisance to humans and animals, they pose a more substantial threat as biological vectors of viral pathogens [1]. Orbiviruses (e.g., BTV and EHDV) are transmitted by Culicoides spp. and threaten wildlife and livestock, especially naïve populations in northern latitudes, such as Ontario, Canada [23]. The health risk to these populations is even greater based on the recent orbivirus incursion into northern latitudes across several continents [18, 23, 37]. Based on these ongoing northern incursions, which have been well documented in the United States [19], we conducted a comprehensive survey of Culicoides spp. from sites throughout southern Ontario, Canada over two field seasons. We observed that within southern Ontario, more northern Culicoides spp. trapping locations had a pattern of seasonal peak abundance in August (2017) and July (2018), and southern locations had abundance peaks in mid-June for both years. Overall, a higher richness of Culicoides spp. (including two species and one species group) were collected in light traps at sites where ovine was the primary livestock type. A known BTV and EHDV vector (C. sonorensis) was among the Culicoides species identified, as well as potential vectors, C. stellifer and C. venustus.

Identifying the seasonal peak abundance (i.e., generation emergence) of targeted vector species of public, livestock, or wildlife health importance can assist in the development of risk management and future surveillance approaches. It can also help identify mitigation strategies, such as adjusting the timing of livestock management activities (e.g., shearing sheep, pasture rotation, moving animals indoors) to minimize skin contact and thus biting [38]. Culicoides spp. data, such as seasonal peak abundance, for Ontario are scarce, and the landscapes and latitudes are highly varied, making it difficult to compare results across studies and regions. For the northern sites in our study, we identified numerous peaks but the overall seasonal abundance peak was in mid- to late summer of both years (i.e., August 2017 and July 2018). Our findings for northern locations differ from the seasonal peaks previously identified in Ontario [39], but resemble those in Northern Ireland and southeast England where some species (e.g., C. obsoletus, subgenus Avaritia) have two to three distinct abundance peaks [40, 41] usually in late July and early August [41]. In our study, seasonal abundance peaked in mid-June in more southern Ontario locations for both years of study, with similar observed abundance peaks as previously described in more eastern Ontario locations. Specifically, Jewiss-Gaines [39] reported numerous sequential, annual (2013–2017), seasonal Culicoides spp. abundance peaks in June in St. Catharines, Ontario. This site, located close to the border with the U.S. (at Niagara Falls, New York), is approximately 300 km northeast of our nearest southern location.

Culicoides spp. reproduction and survivability in any given region are influenced in part by landscape and climatic variables [1, 42,43,44]. Habitat preferences, including host species availability and larval habitat, will impact the ability and frequency of Culicoides reproduction, which in turn will dictate the abundance and regional diversity of Culicoides spp. in a given area and year [41, 45, 46]. We observed higher abundance of some Culicoides spp. at sites where sheep (ovine) were the primary livestock type. While some Culicoides spp. females have shown host species preferences [6, 47], preferences for ovine-occupied habitats have not yet been shown for C. biguttatus, C. stellifer, or subgenus Avaritia within North America. In general, these species are considered mammal-biting generalist feeders, including white-tailed deer in some regions, utilizing a variety of avian and mammalian hosts [6, 46, 48,49,50]. Feeding selection in some cases may be attributed to spatial overlap of vectors and hosts, not the host preference itself [46]. Additionally, site management could be inadvertently increasing the success of Culicoides larval stages. Our observation of increased midge abundance at sites where ovine were the primary livestock type could be due to differences in Ontario livestock management systems between cattle and sheep (e.g., water and waste management systems), how different hosts use the landscape (e.g., their comfort with and thereby proximity to traps), associated landscape differences (e.g., water systems, common ground substrates), or some unrecognized factor(s) (e.g., insecticide/antiparasitic use) unrelated to host type [41, 51].

In addition to landscape, climatic conditions may affect Culicoides spp. abundance [1, 42,43,44]. For example, in our study, temperature appeared to impact the abundance of C. stellifer, subgenus Avaritia, and C. biguttatus. While temperature has been proposed to positively influence Culicoides spp. abundance in some temperate regions [52, 53], there are temperature thresholds at which abundance is negatively impacted for some Culicoides spp. [5]. In our study, daily temperatures did not exceed 31.0 °C so we were not able to establish temperature thresholds for the Culicoides spp. detected. For example, C. biguttatus numbers decreased with increasing seasonal temperatures in Georgia and eastern Tennessee, USA [48, 54], indicating that this vernal species is not tolerant of higher temperatures, and its survival or activity may be negatively impacted by higher temperatures. This could explain why temperature categories from 4 and 8 weeks prior to insect collection appeared to correlate to decreased abundance of C. biguttatus in Ontario in our study.

Additional climatic factors also are important, as higher rainfall amounts can impact breeding and thus Culicoides abundance by lowering the temperature and raising humidity [53, 55]. In our study, rainfall amounts 4 and 8 weeks prior to trapping significantly impacted the abundance of C. biguttatus and was associated with both a decrease in abundance [4 weeks prior (0.1–2.6 mm category), and 8 weeks prior (2.2–72.0 mm category)]. Too much rain may discourage midges from activities such as foraging or mate-seeking [53], which may explain the decrease in abundance of C. biguttatus in the higher rain categories. Culicoides biguttatus tend to emerge early in the season (i.e., spring) and emergence longevity depends on environmental moisture levels [54, 56]. In our study, an increase in rainfall amounts 4 and 8 weeks prior to trapping may have adversely affected C. biguttatus abundance by disrupting breeding sites and inhibiting feeding and mating [53, 54]. In terms of increasing abundance with a moderate increase in rainfall (such as in our study with subgenus Avaritia), Culicoides species do require water/moisture in many cases for development and survival [1, 2, 5, 7]. Our data suggest that the effects of environmental factors such as temperature and precipitation vary by species and species group, and correspond to species-specific phenological and environmental constraints. Additionally, some environmental variables may indirectly impact others, further increasing the complexity of vector–host–virus interactions within the environment. Such additional interactions in these systems are not accounted for in the present analysis but are an important consideration in devising region-specific, vector control strategies aimed at mitigation of virus transmission (such as eliminating/reducing larval development sites).

Despite their importance as vectors of EHDV and BTV, the geographic distribution and abundance of Culicoides spp., as well as species-specific vectorial capacity, are poorly understood [15, 18]. In North America, only two Culicoides spp. have been confirmed as vectors of BTV and EHDV (C. sonorensis and C. insignis) [10, 12, 13]. In Ontario, we identified a small number of C. sonorensis, mainly in southern sites close to livestock. Livestock proximity was not surprising, since C. sonorensis larvae prefer “waste-enhanced mud” (i.e., manure-polluted water) [7, 57, 58]. We identified additional species that may be competent vectors and facilitate EHDV and BTV spread in the region (e.g., C. stellifer, C. spinosus, and C. venustus) [11, 15, 19]. Culicoides stellifer inhabits temperate regions throughout most of the United States (with the exception of the Pacific Northwest) and eastern Canada, from Ontario to Nova Scotia [49, 59]. While C. stellifer was recorded throughout our trapping sites, numbers were lower at southern sites. Culicoides spinosus has been found in Alberta eastward to Nova Scotia and south to Nebraska, Louisiana, and Florida [59]. In our study, C. spinosus was found throughout the study range but was lower in number at northern sites. Culicoides venustus has been documented in Maryland, south to Nebraska, Louisiana, and Florida, and in Ontario eastward to Nova Scotia [59]. We recovered them at multiple study sites in southern Ontario, mainly at more northern locations. Due to their recognized importance to agriculthealth in the U.S., additional research on these Culicoides species is needed [19].

The distribution of Culicoides spp. as well as other arthropod vectors is changing, and in some cases expanding, due to altered landscape and climate dynamics [19, 28, 29, 60]. In particular, C. sonorensis and C. insignis may be undergoing a northward expansion in North America [28, 29]. Over 1400 Culicoides spp. have been documented worldwide, and while characterization of taxonomic diversity, composition, and distribution of many species is ongoing, such baseline information is lacking in many northern latitudes. We identified C. sonorensis at three of our southern Ontario study sites. In Canada, C. sonorensis was previously believed to exist only in western regions, mainly British Columbia and Alberta [26,27,28]. However, C. sonorensis recently was identified in the public health regions of Lambton, Oxford, Hamilton, and Niagara across the southwestern portion of southern Ontario [28]. While we have only confirmed a small number of individuals, our study reinforces the previous findings by identifying C. sonorensis from additional sites in the southwestern portion of southern Ontario (Lambton/Sarnia Fig. 1). Our results suggest that C. sonorensis may be more widespread in the southwestern region of Ontario than previously known. Culicoides sonorensis may have already been present in this area but was not previously identified. Historical surveillance in Ontario has been minimal. Our continued identification of this vector suggests that the province requires continued vigilance and expanded surveillance because this area could be at a higher risk for BTV/EHDV incursion and establishment. There were individuals within subgenus Monoculicoides that could not be further classified in our study (Tables 2, 3, 4). With the advancements in genetic differentiation [30], this could assist future work where hybridization and cryptic species are present/possible.

Our study has limitations common to previous insect-based surveillance studies, including biases associated with trapping (e.g., frequency of trapping, trap light, trap height, attractant used), sampling sites (e.g., habitat type and microhabitats, and proximity to other habitats), and challenges in taxonomic identification. While suction traps are the gold standard for insect surveillance studies, they are inherently biased. Species diversity and composition in a given trap vary based on site selection, trap type (e.g., CDC, OVI [ovitrap], Rothamsted), attractant use (e.g., light [LED/UV], carbon dioxide), and placement (i.e., height) [46, 61,62,63,64,65], thus affecting our understanding of spatial–temporal dynamics. In addition, specific trap types often target a single vector life stage (e.g., larva vs. adult), which may limit understanding of the implications of vector presence in a given region. Our site selections were opportunistic based on voluntary farmer participation and available farm types in our target locations, which created nonuniform coverage of the landscape. The present study targeted adult Culicoides spp. in flight, both through trap type selection and habitat/trap placement, whereas inclusion of larval trapping and resting sites (e.g., tree cover) would have provided a more holistic picture of Culicoides vector biology in the study region. In addition, identifying Culicoides spp. by morphological structural traits requires extensive training and specialized expertise, and occasionally, molecular confirmation. This was the case for the close relatives in subgenus Monoculicoides, C. sonorensis, and C. variipennis and for the subgenus Avaritia which can comprise a number of species. In some cases, we could not confirm the species, which may have resulted in artificially low numbers of C. sonorensis. For subgenus Avaritia, which includes species that are morphologically similar and often co-occur, accurate species identification generally requires specimen dissection and slide mounting to closely examine mouth parts. This process would have not been feasible considering the large number of specimens collected. Additionally, as we grouped our seasonal abundance data for an overall picture of what occurred over trapping seasons, expanding upon this work would provide a more detailed picture of these different species.

Conclusions

We identified and quantified numerous Culicoides species, subgenera, and species groups from different sites across southern Ontario, Canada, and identified environmental variables that could impact regional vector abundance. The presence of Culicoides spp. in the study region overlaps with habitats and landscapes that are home to both domestic and wild animals at risk of infection and disease due to Culicoides spp.-transmitted pathogens, such as EHDV and BTV. In our study, we identified that Culicoides spp. appear to be distinctly spatially and temporally distributed. The livestock species present, temperature, and rainfall appear to have an impact on the abundance of Culicoides biguttatus, C. stellifer, and subgenus Avaritia trapped. A more complete understanding of the diversity and abundance of this important arthropod group, as well as aspects of their biology and the surrounding environment, requires additional work. Future studies in southern Ontario should focus on other Culicoides species of concern (e.g., C. stellifer) and include multiple consecutive (more than 2 years) with year-round sampling seasons. The resulting data would expand upon and improve our understanding of the present study results and assist in the development of risk assessments and mitigation tactics.

Availability of data and materials

All data generated and analyzed during this study are included in this published article.

Abbreviations

BTV:

Bluetongue virus

CDC:

Centers for Disease Control and Prevention

EHDV:

Epizootic hemorrhagic disease virus

CR:

Count ratio

LED:

Light-emitting diode

UV:

Ultraviolet

References

  1. Mellor PS, Boorman J, Baylis M. Culicoides biting midges: their role as Arbovirus vectors. Annu Rev Entomol. 2000;45:307–40.

    Article  CAS  PubMed  Google Scholar 

  2. Carpenter S, Groschup MH, Garros C, Felippe-Bauer ML, Purse BV. Culicoides biting midges, arboviruses and public health in Europe. Antivir Res. 2013;100:102–13.

    Article  CAS  PubMed  Google Scholar 

  3. Ma Y, Xu J, Yang Z, Wang X, Lin Z, Zhao W, et al. A video clip of the biting midge Culicoides anopheles ingesting blood from an engorged Anopheles mosquito in Hainan, China. Parasit Vectors. 2013;6:326.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Borkent A. The subgeneric classification of species of Culicoides—thoughts and a warning. 2016. https://www.inhs.illinois.edu/files/5014/6532/8290/CulicoidesSubgenera.pdf. Accessed 29 Dec 2021.

  5. Purse BV, Carpenter S, Venter GJ, Bellis G, Mullens BA. Bionomics of temperate and tropical Culicoides midges: knowledge gaps and consequences for transmission of Culicoides-borne viruses. Annu Rev Entomol. 2015;60:373–92.

    Article  CAS  PubMed  Google Scholar 

  6. de Martínez- la Puente J, Figuerola J, Soriguer R. Fur or feather? Feeding preferences of species of Culicoides biting midges in Europe. Trends Parasitol. 2015;31:16–22.

    Article  Google Scholar 

  7. Pfannenstiel RS, Mullens BA, Ruder MG, Zurek L, Cohnstaedt LW, Nayduch D. Management of north American Culicoides biting midges: current knowledge and research needs. Vector Borne Zoonotic Dis. 2015;15:374–84.

    Article  PubMed  Google Scholar 

  8. Erram D, Burkett-Cadena N. Laboratory studies on the oviposition stimuli of Culicoides stellifer (Diptera: Ceratopogonidae), a suspected vector of Orbiviruses in the United States. Parasit Vectors. 2018;11:300.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Tanya V, Greiner E, Gibbs EPJ. Evaluation of Culicoides insignis (Diptera: Ceratopogonidae) as a vector of bluetongue virus. Vet Microbiol. 1992;32:1–14.

    Article  CAS  PubMed  Google Scholar 

  10. Tabachnick WJ. Culicoides variipennis and bluetongue-virus epidemiology in the United States. Annu Rev Entomol. 1996;41:23–43.

    Article  CAS  PubMed  Google Scholar 

  11. Smith KE, Stallknecht DE. Culicoides (Diptera: Ceratopogonidae) collected during epizootics of hemorrhagic disease among captive white-tailed deer. J Med Entomol. 1996;33:507–10.

    Article  CAS  PubMed  Google Scholar 

  12. Pfannenstiel RS, Ruder MG. Colonization of bison (Bison bison) wallows in a tallgrass prairie by Culicoides spp (Diptera: Ceratopogonidae). J Vector Ecol. 2015;40:187–90.

    Article  PubMed  Google Scholar 

  13. McGregor BL, Erram D, Alto BW, Lednicky JA, Wisely SM, Burkett-Cadena ND. Vector competence of Florida Culicoides insignis (Diptera: Ceratopogonidae) for epizootic hemorrhagic disease virus serotype-2. Viruses. 2021;13:410.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. McGregor BL, Shults PT, McDermott EG. A review of the vector status of North American Culicoides (Diptera: Ceratopogonidae) for bluetongue virus, epizootic hemorrhagic disease virus, and other arboviruses of concern. Curr Trop Med Rep. 2022;9:130–9.

    Article  PubMed  PubMed Central  Google Scholar 

  15. McGregor BL, Sloyer KE, Sayler KA, Goodfriend O, Campos Krauer JM, Acevedo C, et al. Field data implicating Culicoides stellifer and Culicoides venustus (Diptera: Ceratopogonidae) as vectors of epizootic hemorrhagic disease virus. Parasit Vectors. 2019;12:258.

    Article  PubMed  PubMed Central  Google Scholar 

  16. MacLachlan NJ, Drew CP, Darpel KE, Worwa G. The pathology and pathogenesis of bluetongue. J Comp Path. 2009;141:1–16.

    Article  CAS  PubMed  Google Scholar 

  17. Sterritt WG, Dulac GC. Evolving perceptions of bluetongue: a challenge for government and industry. Can Vet J. 1991;32:109–11.

    Google Scholar 

  18. Pybus MJ, Ravi M, Pollock C. Epizootic hemorrhagic disease in Alberta. Canada J Wild Dis. 2014;50:720–2.

    Article  Google Scholar 

  19. Ruder MG, Lysyk TJ, Stallknecht DE, Foil LD, Johnson DJ, Chase CC, et al. Transmission and epidemiology of bluetongue and epizootic hemorrhagic disease in north America: current perspectives, research gaps, and future directions. Vector Borne Zoonot Dis. 2015;15:348–63.

    Article  Google Scholar 

  20. Gibbs EPJ, Tabachnick WJ, Holt TJ, Stallknecht DE. US concerns over bluetongue. Science. 2008;320:872.

    Article  CAS  PubMed  Google Scholar 

  21. Allison AB, Goekjian VH, Potgieter AC, Wilson W, Johnson D, Mertens PPC, et al. Detection of a novel reassortant epizootic hemorrhagic disease virus in the United States containing RNA segments derived from both exotic and endemic serotypes. J Gen Virol. 2010;91:430–9.

    Article  CAS  PubMed  Google Scholar 

  22. MacLachlan NJ. Global implications of the recent emergence of bluetongue virus in Europe. Vet Clin North Am Food Anim Pract. 2010;26:163–71.

    Article  PubMed  Google Scholar 

  23. Allen SE, Rothenburger JL, Jardine CM, Ambagala A, Hooper-McGrevy K, Colucci N, et al. Epizootic hemorrhagic disease in white-tailed deer. Canada Emerg Infect Dis. 2019;25:832–4.

    Article  PubMed  Google Scholar 

  24. Lorusso A, Cappai S, Loi F, Pinna L, Ruiu A, Puggioni G, et al. First detection of epizootic haemorrhagic disease virus in the European Union, Italy. BioRxiv. 2022. https://doi.org/10.1101/2022.11.23.517495.

    Article  Google Scholar 

  25. MacLachlan NJ, Guthrie AJ. Re-emergence of bluetongue, African horse sickness, and other orbivirus diseases. Vet Res. 2010;41:35.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Downes JA. The Culicoides variipennis complex: a necessary realignment of nomenclature (Diptera: Ceratopogonidae). Can Entomol. 1978;11:63–9.

    Article  Google Scholar 

  27. Lysyk TJ, Dergousoff SJ. Distribution of Culicoides sonorensis (Diptera: Ceratopogonidae) in Alberta. Canada J Med Entomol. 2014;51:560–71.

    Article  CAS  PubMed  Google Scholar 

  28. Jewiss-Gaines A, Barelli L, Hunter FF. First records of Culicoides sonorensis (Diptera: Ceratopogonidae), a known vector of bluetongue virus, in southern Ontario. J Med Entomol. 2017;54:757–62.

    CAS  PubMed  Google Scholar 

  29. Vigil SL, Ruder MG, Shaw D, Wlodkowski J, Garrett K, Walter M, et al. Apparent range expansion of Culicoides (Hoffmania) insignis (Diptera: Ceratopogonidae) in the southeastern United States. J Med Entomol Volume. 2018;55:1043–6.

    Article  Google Scholar 

  30. Shults P, Moran M, Blumenfeld AJ, Vargo EL, Cohnstaedt LW, Eyer PA. Development of microsatellite markers for population genetics of biting midges and a potential tool for species identification of Culicoides sonorensis Wirth and Jones. Parasit Vectors. 2022;15:69.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Allen SE, Vigil SL, Jardine CM, Furukawa-Stoffer T, Colucci N, Ambagala A, et al. New distribution records of biting midges of the genus Culicoides (Diptera: Ceratopogonidae) Latreille, Culicoides bergi and Culicoides baueri, in southern Ontario. Canada J Med Entomol. 2022;59:1467–72.

    Article  CAS  PubMed  Google Scholar 

  32. Central Massachusetts Mosquito Control Project. Central Mass. EPI week calendars 2008–2021. 2021. https://www.cmmcp.org/mosquito-surveillance-data/pages/epi-week-calendars-2008-2021. Accessed 29 Dec 2021.

  33. Becker ME, Roberts J, Schroeder ME, Gentry G, Foil LD. Prospective study of epizootic hemorrhagic disease virus and bluetongue virus transmission in captive ruminants. J Med Entomol. 2020;57:1277–85.

    Article  CAS  PubMed  Google Scholar 

  34. Quaglia AI, Blosser EM, McGregor BL, Runkel AE, Sloyer KE, Erram D, et al. Tracking community timing: Pattern and determinants of seasonality in Culicoides (Diptera: Ceratopogonidae) in northern Florida. Viruses. 2020;12:931.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Rigot T, Drubbel MV, Delécolle JC, Gilbert M. Farms, pastures and woodlands: the fine-scale distribution of Palearctic Culicoides spp. biting midges along an agro-ecological gradient. Med Vet Entomol. 2013;27:29–38.

    Article  CAS  PubMed  Google Scholar 

  36. Government of Canada. Past weather and climate—Historical data. 2019. https://climate.weather.gc.ca/historical_data/search_historic_data_e.html. Accessed May 2019.

  37. Stallknecht DE, Allison AB, Park AW, Phillips J, Goekjian VH, Nettles VF, et al. Apparent increase of reported hemorrhagic disease in the midwestern and northeastern United States. J Wildl Dis. 2015;51:348–61.

    Article  PubMed  Google Scholar 

  38. Hope A, Gubbins S, Sanders C, Barber J, Stubbins F, Baylis M, et al. Sheep breed and shearing influences attraction and blood-feeding behaviour of Culicoides (Diptera: Ceratopogonidae) on a UK farm. Parasit Vectors. 2018;11:473.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Jewiss-Gaines A. A study of biting midge populations and an assessment of bluetongue virus presence in southern Ontario, with a visual dichotomous key to the north American genera of Ceratopogonidae. St. Catharines, Ontario, Canada: Brock University; 2018.

    Google Scholar 

  40. Holmes PR, Boorman JPT. Light and suction trap catches of Culicoides midges in southern England. Med Vet Entomol. 1987;1:349–59.

    Article  CAS  PubMed  Google Scholar 

  41. Jess S, Thompson GM, Clawson S, Forsythe IWN, Rea I, Gordon AW, et al. Surveillance of biting midges (Culicoides spp.) in northern Ireland: influence of seasonality, surrounding habitat and livestock housing. Med Vet Entomol. 2018;32:48–60.

    Article  CAS  PubMed  Google Scholar 

  42. Searle KR, Blackwell A, Falconer D, Sullivan M, Butler A, Purse BV. Identifying environmental drivers of insect phenology across space and time: Culicoides in Scotland as a case study. Bull Entomol Res. 2012;103:155–70.

    Article  PubMed  Google Scholar 

  43. Elbers ARW, Koenraad CJM, Meiswinkel R. Mosquitoes and Culicoides biting midges: vector range and the influence of climate change. OIE Rev Sci Tech. 2015;34:123–37.

    Article  CAS  Google Scholar 

  44. Brand SPC, Keeling MJ. The impact of temperature changes on vector-borne disease transmission: Culicoides midges and bluetongue virus. J R Soc Interface. 2017;14:20160481.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Purse BV, Falconer D, Sullivan MJ, Carpenter S, Mellor PS, Piertney SB, et al. Impacts of climate, host and landscape factors on Culicoides species in Scotland. Med Vet Entomol. 2012;26:168–77.

    Article  CAS  PubMed  Google Scholar 

  46. McGregor BL, Runkel AE, Wisely SM, Burkett-Cadena ND. Vertical stratification of Culicoides biting midges at a Florida big game preserve. Parasit Vectors. 2018;11:505.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Borkent A. World species of biting midges (Diptera: Ceratopogonidae). Bull of the AMNH. 1997;233. https://digitallibrary.amnh.org/handle/2246/1622

  48. Brickle DS, McKeever S, Hagan DV. Bionomics of bloodsucking midges (Diptera: Ceratopogonidae: Culicoides) on the coastal plain of Georgia, USA. Russian Entomol. 2008;17:41–61.

    Google Scholar 

  49. Sloyer KE, Acevedo C, Runkel AE, Burkett-Cadena ND. Host associations of biting midges (Diptera: Ceratopogonidae: Culicoides) near sentinel chicken surveillance locations in Florida, USA. J Am Mosquito Contr. 2019;35:200–6.

    Article  Google Scholar 

  50. McGregor BL, Stenn T, Sayler KA, Blosser EM, Blackburn JK, Wisely SM, et al. Host use patterns of Culicoides spp. biting midges at a big game preserve in Florida, U.S.A., and implications for the transmission of orbiviruses. Med Vet Entomol. 2019;33:110–20.

    Article  CAS  PubMed  Google Scholar 

  51. Sloyer KE, Burkett-Cadena ND. Development and field evaluation of a motion sensor activated suction trap to study vector-host interactions. Methods Ecol Evol. 2020;12:204–11.

    Article  Google Scholar 

  52. Ortega MD, Lloyd JE, Holbrook FR. Seasonal and geographical distribution of Culicoides imicola Kieffer (Diptera: Ceratopogonidae) in southwestern Spain. J Am Mosq Contol Assoc. 1997;13:227–32.

    CAS  Google Scholar 

  53. Gusmão GMC, Brito GA, Moraes LS, Bandeira MDCA, Rebelo JMM. Temporal variation in species abundance and richness of Culicoides (Diptera: Ceratopogonidae) in a tropical equatorial area. J Med Entomol. 2019;56:1013–8.

    Article  PubMed  Google Scholar 

  54. Root D, Gerhardt R. Seasonal emergence patterns of Culicoides (Diptera: Ceratopogonidae) in eastern Tennessee. J Agric Entomol. 1991;8:127–35.

    Google Scholar 

  55. Carrasquilla MC, Guhl F, Zipa Y, Ferro C, Pardo RH, Cabrera OL, et al. Breeding sites of Culicoides pachymerus Lutz in Magdalena River basin. Colombia Mem Inst Oswaldo Cruz. 2010;105:216–9.

    Article  PubMed  Google Scholar 

  56. Blanton FS, Wirth WW. The sand flies (Culicoides) of Florida (Diptera: Ceratopogonidae). Arthropods Fla Neighb Land Areas. 1979;10:1–204.

    Google Scholar 

  57. Mullens B. A quantitative survey of Culicoides variipennis (Diptera: Ceratopogonidae) in dairy waste water ponds in southern California. J Med Entomol. 1989;26:559–65.

    Article  CAS  PubMed  Google Scholar 

  58. Gerry AC, Mullens BA, MacLachlan NJ, Mecham JO. Seasonal transmission of bluetongue virus by Culicoides sonorensis (Diptera: Ceratopogonidae) at a southern California dairy and evaluation of vectorial capacity as a predictor of bluetongue virus transmission. J Med Entomol. 2001;38:197–209.

    Article  CAS  PubMed  Google Scholar 

  59. Borkent A, Grogan WL. Catalog of the new world biting midges north of Mexico (Diptera: Ceratopogonidae). Zootaxa. 2009;48:1–48.

    Article  Google Scholar 

  60. Jacquet S, Huber K, Pages N, Talavera S, Burgin LE, Carpenter S, et al. Range expansion of the bluetongue vector, Culicoides imicola, in continental France likely due to rare wind-transport events. Sci Rep. 2016;6:27247.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  62. McDermott EG, Mayo CE, Gerry AC, Laudier D, MacLachlan NJ, Mullens BA. Bluetongue virus infection creates light averse Culicoides vectors and serious errors in transmission risk estimates. Parasit Vectors. 2015;8:460.

    Article  PubMed  PubMed Central  Google Scholar 

  63. Venter GJ, Boikanyo SNB, Majatladi DM, Morey L. Influence of carbon dioxide on numbers of Culicoides midges collected with suction light traps in South Africa. Med Vet Entomol. 2016;30:117–22.

    Article  CAS  PubMed  Google Scholar 

  64. Walgama RS, Lysyk TJ. Evaluating the addition of CO2 to black light traps for sampling Culicoides (Diptera: Ceratopogonidae) in Alberta. J Med Entomol. 2019;56:169–80.

    Article  CAS  PubMed  Google Scholar 

  65. McDermott EG, Lysyk TJ. Sampling considerations for adults and immature Culicoides (Diptera: Ceratopogonidae). J Insect Sci. 2020;20:1–11.

    Article  Google Scholar 

Download references

Acknowledgements

We are grateful to Ontario livestock farmers for their participation and permission to access lands. To the Ontario Ministry of Agriculture, Food and Rural Affairs, particularly Jocelyn Jansen. We thank Paul Oesterle, Tami Sauder, Yuqing Sun, Barret Foster, Alessandra Chek-Harder, Dr. Joseph Wilson, and Will Heibein for logistical support and laboratory/field assistance.

Funding

This study was funded by the Ontario Ministry of Agriculture, Food and Rural Affairs, University of Guelph Partnership (UofG2015-2212), the Canadian Foundation for Innovation (RGPIN-2015-04088), the Ontario Veterinary College, Ontario Sheep Marketing Agency, and Natural Science and Engineering Research Council of Canada.

Author information

Author notes

  1. Samantha E. Allen

    Present address: Wyoming Game and Fish Department, Veterinary Services, Laramie, USA

Authors and Affiliations

  1. Department of Pathobiology, Ontario Veterinary College, University of Guelph, Guelph, Canada

    Samantha E. Allen & Claire M. Jardine

  2. Canadian Wildlife Health Cooperative, Ontario Veterinary College, University of Guelph, Guelph, Canada

    Samantha E. Allen & Claire M. Jardine

  3. Southeastern Cooperative Wildlife Disease Study, College of Veterinary Medicine, University of Georgia, Athens, USA

    Stacey L. Vigil, Mark G. Ruder & Nicole M. Nemeth

  4. Canadian Food Inspection Agency, National Centre for Animal Diseases, Lethbridge, Canada

    Tara Furukawa-Stoffer & Nicole Colucci

  5. Canadian Food Inspection Agency, National Centre for Foreign Animal Disease, Winnipeg, Canada

    Aruna Ambagala

  6. Department of Population Medicine, Ontario Veterinary College, University of Guelph, Guelph, Canada

    David L. Pearl

  7. Department of Pathology, University of Georgia, Athens, USA

    Nicole M. Nemeth

Authors
  1. Samantha E. Allen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stacey L. Vigil
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tara Furukawa-Stoffer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nicole Colucci
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Aruna Ambagala
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. David L. Pearl
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mark G. Ruder
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Claire M. Jardine
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Nicole M. Nemeth
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

SEA, MGR, CMJ, and NMN designed and developed the study. SEA collected the field samples. SEA, SLV, TFS, NC, and AA processed the field samples. SEA and DLP analyzed the data. SEA and NMN drafted the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Samantha E. Allen.

Ethics declarations

Ethics approval and consent to participate

Written consent from landowners (for insect trapping) was acquired prior to the start of the study.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Allen, S.E., Vigil, S.L., Furukawa-Stoffer, T. et al. Abundance and diversity of Culicoides Latreille (Diptera: Ceratopogonidae) in southern Ontario, Canada. Parasites Vectors 16, 201 (2023). https://doi.org/10.1186/s13071-023-05799-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s13071-023-05799-w

Keywords

Parasites & Vectors

ISSN: 1756-3305

Contact us