Abstract
Entomological monitoring was carried out from April 2007 to May 2008 at 20 locations in the areas of Lower Saxony, Schleswig-Holstein, Hamburg, and Bremen. A total number of 26 Culicoides species were sampled by light traps during the first week of every month. Culicoides diversity was highest in summer, achieving more than 20 species and genera per month. Numbers of Culicoides were highest in spring and summer with a maximum of 325,000 individuals in May 2008 at a single location. During the winter, the number of individuals decreased considerably, but few individuals of Culicoides were present even during the coldest months in January and February with Culicoides obsoletus remaining the only species complex. The total number of Ceratopogonidae and the number of individuals from C. obsoletus complex and Culicoides pulicaris complex were significantly correlated with temperature almost at any date and location.
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Introduction
The data we present in this publication originate from 20 out of 28 locations chosen for entomologic monitoring of Culicoides in the areas of Lower Saxony, Schleswig-Holstein, Hamburg, and Bremen. The first occurrence of bluetongue disease (BTD) in Germany dates back to 21 October 2006. At that time, the first infections were diagnosed on a farm in the Aachen area. Despite wide-ranging restricted areas established by the authorities soon after the onset of the disease, BTD spread quite rapidly north and especially eastwards.
In spring 2007, an entomological monitoring project was started in 89 geographic areas of Germany in order to gain adequate data on the distribution of Culicoides species, of which at least the Culidoides obsoletus and Culicoides pulicaris complex were considered to be potent BT virus vector species. Additionally, this monitoring program was planned to provide useful information on the biology and vector capacity of Culicoides species.
Prior to the start of this monitoring project in March 2007, BTD had already been diagnosed in Lower Saxony. While screening BT virus antibodies during a specific survey, 21 infections were noticed in winter 2007/2008. BTD specialists and veterinary medics thus presume the infection of cows to date back to the previous year (Dr. Schmedt auf der Günne, LAVES, acromatic, November 2008).
Materials and methods
All traps were placed in the immediate vicinity of the predominant residences of cows. Thirteen light traps were placed either adjacent to the barn (0–3 m distance) or in its entrance area (two traps). Another five traps were placed 5 and 19 m away from the barn. These traps were also considered to be close to the cows, as they stood adjacent to the dirt road which was used by the cows at least twice a day (Table 1).
All traps were installed at 1.5 m above the ground. In the immediate vicinity of the trap, a photo sensor and a data logger were installed. The photo sensor was adjusted to illuminate the black light lamp at sunset. The data logger recorded air temperature and humidity in 4-h intervals. The traps had to be shielded against rain as effectively as possible. Therefore, they either were fixed to a free-standing wooden construction, which was stuck in the ground next to the barn (Fig. 1, left picture) or were fixed directly to a wall of the barn (Fig. 1, right picture).
In April 2007, light traps were emptied only once at the end of the catch period (first week) at every location. Insects caught until the end of the seventh night were emptied immediately, put into 70% ethanol, and transported to the laboratory. This monthly catch rhythm was maintained for the whole catch period till May 2008 at four locations (NI CE, NI H, NI HI, and NI SHG). At the other locations, from May 2007 to May 2008, insects were emptied and put into 70% ethanol diurnal before sunset just before start of the next catch night (Table 2).
In the laboratory, the material was presorted in order to differentiate Ceratopogonidae from other insects. Individuals of the C. obsoletus and C. pulicaris species complex were differentiated from other Ceratopogonidae. While males were only counted, females were counted and differentiated according to the criteria: gravidity and no blood ingestion/blood ingestion. Aliquots of the Culicoides were sent to Dr. D. Werner (ZALF, Müncheberg) for determination of species level.
Results
From April 2007 to May 2008, a total of 26 Culicoides species (det. D. Werner 2007–2008) were collected in our area of investigation (Lower Saxony, Germany). Additionally, we found many undetermined individuals belonging to the genera Atrichopogon and Forcipomyia and huge amounts of other insects (Table 3).
Culicoides diversity was highest during June and July 2007 (Fig. 2), achieving 21 species and genera per month. Although the number of species and genera subsequently decreased, up to 16 or 17 species and genera per month were caught until October 2007 and again in May 2008. Culicoides diversity was lowest in January and February 2007, when C. obsoletus remained the only species complex caught in our light traps.
The total amount of individuals caught by light trap investigations at 20 locations in Lower Saxony (Germany) achieved maxima of 140,000 individuals in August 2007 and 325,000 individuals in May 2008. During the winter time, the number of individuals decreased considerably (Fig. 3). However, seven to 256 individuals per month were trapped even in the winter months (December 2007–April 2008). Some Ceratopogonidae were caught even during the coldest months (January and February) at the locations CE, DH, EL H, HB, HH, NI, VEC, and WST.
While the C. obsoletus complex dominated in summer, more individuals of the C. pulicaris complex were trapped in spring (Fig. 4). However, when interpreting these results, it has to be considered that most of the C. pulicaris individuals originated from two locations only: NI AUR and HH HH.
The highest number of Culicoides was achieved at the location NI AUR. In May 2008, a total of approximated 237,000 Culicoides was caught at this location and 90% of the individuals belong to the C. pulicaris complex (Fig. 5). There was no other location and no other sampling date with such high numbers and such a clear dominance of the C. pulicaris complex. At the location HH HH, the individuals of the C. pulicaris complex achieved about 60% of the fauna, while the number of individuals of the C. obsoletus complex was much lower, although they dominated at all other locations. The total numbers of other species of the Ceratopogonidae were also much lower.
However, the sex ratio in the C. pulicaris complex was often unbalanced. From August 2007 to November 2007 and in May 2008, only about 40% of the individuals were females (Fig. 7). While in April and May 2007 and in April 2008, exclusively females without blood ingestion were trapped, the proportion of females trapped with blood ingestion increased during summer. From June to August 2007 and from September 2007 to January 2008, almost 10–30% and 15–50%, respectively, of the females already had ingested blood (Fig. 7).
The sex ratio in the C. obsoletus complex was more or less balanced with only minimal surplus of males in some months. During the whole period of investigation, we found females that already had ingested blood with the lowest numbers in spring (≤10% of females in April, May 2007, and March 2008) and about 20–90% of the females in the other months (Fig. 6). The maximum of engorged or partly engorged females (90% of females) could be observed in November 2007. Figures 6 and 7 again highlight that the few individuals caught in winter predominantly belong to the C. obsoletus complex. At least in January and February, no individuals of the C. pulicaris complex were found.
The total number of Ceratopogonidae and the number of individuals from both species complexes were significantly correlated with temperature at almost any date and location. Significant correlations exist between Ceratopogonid numbers and mean, maximum, and minimum temperature (Table 4).
Discussion
Havelka and Aguilar (1999) named a total of 332 species of Ceratopogonidae as members of the German Ceratopogonid fauna, 57 of which are Culicoides. Except for Culicoides puncticollis (Becker), all of the 20 species we found are named on this list, i.e., were already known to occur in Germany. According to the Institute for Animal Health (Great Britain) (2008), C. puncticollis (Becker) occurs infrequently in Northern Europe but is more common in the Mediterranean, the Middle East, and North Africa.
Although not all our samples could be determined to species level, we estimate that more than 20 species are present in our study area. Currently, it is not clear whether Culicoides lupicaris (Downes and Kettle) can be separated from C. delta (Edwards). Havelka and Aguilar (1999) mention both of them to occur in Germany. On the other hand, Borkent (2008) treats C. lupicaris as a synonym of C. deltus. According to the information provided by the Institute for Animal Health (Great Britain) (2008), C. lupicaris and C. delta may likely be treated as synonyms (http://www.iah.ac.uk/bluetongue/culicoides/deltus.html).
Starting this project, we expected a correlation between air temperature and population development of Ceratopogonidae. It was, therefore, not surprising to find peak numbers of Culicoides in August and a significant correlation of air temperature with the number of Culicoides.
However, we did not anticipate so many species to be still present in midwinter, when we caught a total of 13 Ceratopogonid species in November 2007 and six Ceratopogonid species even in December 2007. We also did not expect active males and females even in the coldest months of our investigation period, i.e., January and February 2008. Males and females of C. obsoletus were trapped during these rainy and stormy months. We conclude that C. obsoletus is the most robust species, which might be a year-round active vector of the bluetongue virus, or at least one of them. Further investigation is necessary to determine if C. obsoletus is reproducing even in winter or if the adults hibernate at adequate sites.
Further studies will also have to reveal possible effects of trap location on the amount and composition of Culicoides fauna caught in our traps. If temperature dependency of Culicoides development and activity is actually as strong as our correlations suggest, the weekly sampling we carried out may cause overestimation or underestimation. Consequently, seasonal, annual, and regional variations should be taken into account. The annual deviations are most pronounced if the May samples are compared: The number of individuals in May 2008 was more than five times the height of the May samples of the previous year.
Concerning the temperature dependency, we also have to be aware of regional differences as well as effects of light trap position, possibly causing differences in numbers and composition of our light trap samples. But currently, too little is known on the biology of most of the species we found in our light traps.
Regardless of the species-specific differences in habitat preferences and the regional differences in habitat conditions, we were surprised to notice the dominance of the C. obsoletus species complex. At more than half of our study locations and for most of the year, the C. obsoletus complex dominated by number. On the other hand, we also wonder what might have caused the huge number of C. pulicaris at a few of the other locations.
Referring to literature (Kampen and Kiel 2006; Olbrich 1987) several habitat types should have been suitable breeding places, but niche confinement and niche selection of most species is not known in detail. However, even though the ecological parameters controlling the habitat selection and the population development of certain Culicoides species are not known in detail, it has to be assumed that aspects of landscape ecology as well as human impacts could have important effects on the distribution and population development. However, we are currently not in a position to relate Culicoides faunal difference to ecological aspects and differentiate natural ecological parameters from the effects of farm management, e.g., manure management.
References
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Acknowledgement
We are grateful to Dr. H.-J. Bätza (BMELV) who initiated this study. Many thanks to all the assistants for their tireless effort in sorting the insects and to Dr. Doreen Werner for the determination. Sincerest thanks also are given to the 20 farmer families who supported our studies for 1.5 years. Without their helpful assistance, this monitoring would not have been realized. Furthermore, we are grateful to Dr. Freise and Dr. Schmedt auf der Günne (LAVES) for supporting our study and responding to all our questions.
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An erratum to this article can be found at http://dx.doi.org/10.1007/s00436-009-1464-3
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Kiel, E., Liebisch, G., Focke, R. et al. Monitoring of Culicoides at 20 locations in northwest Germany. Parasitol Res 105, 351–357 (2009). https://doi.org/10.1007/s00436-009-1409-x
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DOI: https://doi.org/10.1007/s00436-009-1409-x