Diversity, Abundance and Host Preference of Culicoides (Diptera: Ceratopogonidae), Potential Vectors and Nuisance Insect in Zoo Park Košice, Slovakia
Main Article Content
Abstract
Biting midges of the genus Culicoides (Diptera: Ceratopogonidae) were captured in the course of three seasons (2017–2020) in the Zoo Košice. The total number of captured individuals was 5,667 biting midges, and 12 species of Culicoides were identified, while the most frequently captured and the most populous species were C. obsoletus/C. scoticus, C. furcillatus, and C. festivipennis. The most frequent hosts on which the biting midges were blood-feeding were humans (Homo sapiens), Burchell's zebra (Equus quagga burchellii), and domestic cow (Bos taurus). This is the first study to confirm a wide range of biting midges species in a zoo which are capable of using not only animals as their hosts, but also humans, in whom a bite may induce an allergic reaction. More than 80% of the fauna of biting midges in the Zoo Košice represented Culicoides obsoletus/C. scoticus, which are in the Central Europe regarded as the potential vectors of arboviruses, to which primarily ruminants are highly susceptible.
Keywords:
biting midges, species composition, blood feeding, exotic animals
Article Details
How to Cite
KASICOVA, Zuzana et al.
Diversity, Abundance and Host Preference of Culicoides (Diptera: Ceratopogonidae), Potential Vectors and Nuisance Insect in Zoo Park Košice, Slovakia.
Medical Research Archives, [S.l.], v. 9, n. 6, june 2021.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/2398>. Date accessed: 05 nov. 2024.
doi: https://doi.org/10.18103/mra.v9i6.2398.
Section
Research Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
1. Swanson AD, Kapaldo NO, Maki E, Carpenter JW, Conhstaedt LW. Diversity and abudance of nonculicid biting flies (Diptera) in a zoo enviroment. Journal of the American mosquito control association. 2018; 34(4): 265–271.
2. Mellor PS, Boorman J. Multiplication of bluetongue virus in Culicoides nubeculosus (Meigen) simultaneously infected with the virus and the microfilariae of Onchocerca cervicalis (Railliet & Henry). Annals of Tropical Medicine & Parasitology. 1980; 74(4): 463–469. doi: 10.1080/00034983.1980.11687368
3. Dohnal J, Blinn J, Vahl G, Schulz-key H. Distribution of microfilariae of Onchocerca lienalis and Onchocerca gutturosa in the Skin of cattle in Germany and their development in Simulium ornatum and Culicoides nubeculosus following artificial infestation. Veterinary Parasitology. 1990; 36(3-4): 325–332. doi: 10.1016/0304-4017(90)90044-C
4. Wang R, Yu ZC, Luo XP, Chen LJ, Shao GY, Yang XY. Survey of infection and determination of the transmission vector of Onchocerca fasciata in camels (Camelus bactrianus) in Inner Mongolia, China. Medical and Veterinary Entomology. 2019; 34: 59–68.
5. Cambra-Pellejà M, Gandasegui J, Balaña-Fouce R, Muñoz J, Martínez-Valladares M. Zoonotic Implications of Onchocerca Species on Human Health. Pathogens. 2020; 9: 761. doi:10.3390/pathogens9090761
6. Gumisiriza N, Mubiru F, Siewe Fodjo JN, Mbonye Kayitale M, Hotterbeekx A, Idro R, Makumbi I, Lakwo T, Opar B, Kaducu J, et al. Prevalence and incidence of nodding syndrome and other forms of epilepsy in onchocerciasis-endemic areas in northern Uganda after the implementation of onchocerciasis control measures. Infect. Dis. Poverty. 2020; 9: 12. doi: 10.1186/s40249-020-0628-3
7. Mellor PS. Studies on Onchocerca cervicalis Railliet and Henry 1910: I. Onchocerca cervicalis in British horses. J. Helminthol. 1973; 47: 97–110.
8. Foil LD, Kleir TR, Miller RI, Foil CS, French DD, Smith JN. Seasonal changes in density and tissue distribution of Onchocerca cervicalis microfilariae in ponies and related changes in Culicoides variipennis populations in Louisiana. J. Parasitol. 1987; 73: 320–326.
9. El Sinnary K, Hussein HS. Culicoides kingi, Austen: A vector of Onchocerca gutturosa (Neumann, 1910) in the Sudan. Ann. Trop. Med. Parasitol. 1980; 74: 655–656.
10. Scott DM, Griffin WHCE. Skin immune system and allergic skin diseases. In: Saunders W. (Ed.), Small Animal Dermatology. 2001; 543–666.
11. Schaffartzika A, Hamzab E, Jandab J, Crameria R, Martib E, Rhyner C. Equine insect bite hypersensitivity: What do we know? Veterinary Immunology and Immunopathology. 2012; 147: 113– 126.
12. Crilly JP, Nuttall T, del Pozo J, Hopker A, Tomlinson M, Sargison N. Hypersensitivity to Culicoides midges causing seasonal dermatitis in sheep. Veterinary Parasitology: Regional Studies and Reports. 2016; 3–4: 53–56. doi: 10.1016/j.vprsr.2016.06.001
13. Slama D, Haouas N, Mezhoud H, Babba H, Chaker E. Blood meal analysis of Culicoides (Diptera: Ceratopogonidae) in central Tunisia. PLoS One. 2015; 10 (3): doi.org/10.1371/journal.pone.0120528.
14. Keesing F, Holt RD, Ostfeld RS. Effects of species diversity on disease risk. Ecol Lett. 2006; 9: 485–498.
15. Goffredo M, Meiswinkel R. Entomological surveillance of bluetongue in Italy: methods of capture, catch analysis and identification of Culicoides biting midges. Vet. Ital. 2004; 40: 260–265.
16. Delécolle J.-C.: Nouvelle contribution à l’étude systematique et iconographique des espèces du genre Culicoides (Diptera: Ceratopogonidae) du nord-est de la France. Université Louis Pasteur de Strasbourg. 1985.
17. Mathieu B, Cetre-Sossah C, Garros C, Chavernac D, Balenghien T, Carpenter S, Setier-Rio ML, Vignes-Lebbe R, Ung V, Candolfi E, Delécolle JC. Development and validation of IIKC: an interactive identification key for Culicoides (Diptera: Ceratopogonidae) females from the Western Palaearctic region. Parasites & Vectors, 2012; 5, 137.
18. Dyce AL. The recognition of nulliparous and parous Culicoides (Diptera: Ceratopogidae) without dissection. Journal of the Australian Entomology Society. 1969; 8:11–15.
19. Rádrová J, Seblová V, Votýpka J. Feeding behavior and spatial distribution of Culex mosquitoes (Diptera: Culicidae) in wetland areas of the Czech Republic. Journal Medical Entomology. 2013; 50, 1097–104.
20. Adler PH, Tuten HC, Nelder MP. Arthropods of medico veterinary importance in zoos. Annu Rev Entomol. 2011; 56:123–142.
21. Puente MJ, Ruiz S, Soriguer R, Figuerola J. Effect of blood meal digestion and DNA extraction protocol on the success of blood meal source determination in the malaria vector Anopheles atroparvus. Malaria journal. 2013; 12(1): 109.
22. Sandres CJ, Shortall CR, Gubbins S, Burgin L, Gloster J, Harrington R, Reynolds D, Mellor P, Carpenter S. Influence of season and meteorological parameters on flight activity of Culicoides biting midges. Journal of Applied Ecology. 2011; 48: 1355–1364.
23. Bursell E. Enviromental aspects: Humidity. Rockstein, ed. Physiology of the Insecta. Academic Press, New York. 1964; 324–358.
24. Valkiúnas G. Avian malaria parasites and other haemosporidia. CRC PRESS. 2004; 946 pp. ISBN: 9780415300971
25. Synek P, Munciinger P, Albrecht T, Votýpka J. Avian haemosporidians in haematophagous insects in the Czech Republic. Parasitol Res. 2013; 112: 839–845.
26. Alarcon S D, Havelka P, Pineda E, Segelbacher G, Schaefer M. Urban forests as hubs for novel zoonosis: blood meal analysis, seasonal variation in Culicoides (Diptera: Ceratopogonidae) vectors, and avian haemosporidians. Parasitology. 2013; 140 (14): 1799–810. doi: 10.1017/S0031182013001285.
27. Bobeva A, Zehtindjiev P, Ilieva M, Dimitrov D, Mathis A, Bensch S. Host preferences of ornithophilic biting midges of the genus Culicoides in the Eastern Balkans. Medical and Veterinary Entomology. 2015; 29, 290–296.
28. Nelder PM, Swanson AD, Adler PH, Grogan LW. Biting midges of the genus Culicoides in South Carolina zoos. J Insect Sci. 2010; 10, 55. doi: 10.1673/031.010.5501
29. Sarvašová A, Kočišová A, Candolfi E, Mathieu B. Description of Culicoides (Culicoides) bysta n. sp., a new member of the Pulicaris group (Diptera: Ceratopogonidae) from Slovakia. Parasites & Vectors. 2017; 10, 279.
30. Englad EM, Pearce-Kelly P, Brugman AV, King S, Gubbins S, Sach F, Sanders JCH, Masters JN, Denison E, Carpenter S. Culicoides species composition and molecular identification of host blood meals at two zoos in the UK. Parasites & Vectors. 2020; 13, 139. doi.org/10.1186/s13071-020-04018-0
31. Beaver PC, Horner GS, Bilos JZ. Zoonotic onchocercosis in a resident of Illinois and observations on the identification of Onchocerca species. Am J Trop Med Hyg. 1974; 23, 595–607.
32. Koehsler M, Soleiman A, Aspöck H, Auer H, Walochnik J. Onchocerca jakutensis filariasis in humans. Emerg Infect Dis. 2007; 13,1749–52.
33. Orihel TC, Eberhard ML. Zoonotic filariasis. Clin. Microbiol. Rev. 1998; 11, 366–381.
34. Pampiglione S, Vakalis N, Lyssimachou A, Kouppari G, Orithel TC. Subconjunctival zoonotic Onchocerca in an Albanian man. Ann Trop Med Parasitol. 2001; 95, 827–832.
35. Sallo F, Eberhard ML, Fok E, Baska F, Hatvani I. Zoonotic intravitreal Onchocerca in Hungary. Ophthalmology. 2005; 112, 502–504.
36. Wesołowska M, Zając‑Pytrus H, Masny A, Pytrus W, Knysz B, Golab E, Sałamatin R. Onchocerca jakutensis ocular infection in Poland: a new vector‑borne human health risk? Parasites & Vectors. 2020; 13, 61. doi.org/10.1186/s13071-020-3925-6
37. Wright RW, McLean M, Neafie RC, Markman AW. Zoonotic onchocerciasis of the shoulder: A case report. The Journal of Bone and Joint Surgery. 2002; 84, 627-629.
38. Cambra-Pellejà M, Gandasegui J, Balaña-Fouce R, Muñoz J, Martínez-Valladares M. Zoonotic implications of Onchocerca species on human health. Pathogens. 2020; 9, 761. doi:10.3390/pathogens9090761
39. Stavrou A, Daly JM, Maddison B, Gough K, Tarlinton R. How is Europe positioned for a re-emergence of Schmallenberg virus? Veterinary Journal. 2017; 230, 45–51.
2. Mellor PS, Boorman J. Multiplication of bluetongue virus in Culicoides nubeculosus (Meigen) simultaneously infected with the virus and the microfilariae of Onchocerca cervicalis (Railliet & Henry). Annals of Tropical Medicine & Parasitology. 1980; 74(4): 463–469. doi: 10.1080/00034983.1980.11687368
3. Dohnal J, Blinn J, Vahl G, Schulz-key H. Distribution of microfilariae of Onchocerca lienalis and Onchocerca gutturosa in the Skin of cattle in Germany and their development in Simulium ornatum and Culicoides nubeculosus following artificial infestation. Veterinary Parasitology. 1990; 36(3-4): 325–332. doi: 10.1016/0304-4017(90)90044-C
4. Wang R, Yu ZC, Luo XP, Chen LJ, Shao GY, Yang XY. Survey of infection and determination of the transmission vector of Onchocerca fasciata in camels (Camelus bactrianus) in Inner Mongolia, China. Medical and Veterinary Entomology. 2019; 34: 59–68.
5. Cambra-Pellejà M, Gandasegui J, Balaña-Fouce R, Muñoz J, Martínez-Valladares M. Zoonotic Implications of Onchocerca Species on Human Health. Pathogens. 2020; 9: 761. doi:10.3390/pathogens9090761
6. Gumisiriza N, Mubiru F, Siewe Fodjo JN, Mbonye Kayitale M, Hotterbeekx A, Idro R, Makumbi I, Lakwo T, Opar B, Kaducu J, et al. Prevalence and incidence of nodding syndrome and other forms of epilepsy in onchocerciasis-endemic areas in northern Uganda after the implementation of onchocerciasis control measures. Infect. Dis. Poverty. 2020; 9: 12. doi: 10.1186/s40249-020-0628-3
7. Mellor PS. Studies on Onchocerca cervicalis Railliet and Henry 1910: I. Onchocerca cervicalis in British horses. J. Helminthol. 1973; 47: 97–110.
8. Foil LD, Kleir TR, Miller RI, Foil CS, French DD, Smith JN. Seasonal changes in density and tissue distribution of Onchocerca cervicalis microfilariae in ponies and related changes in Culicoides variipennis populations in Louisiana. J. Parasitol. 1987; 73: 320–326.
9. El Sinnary K, Hussein HS. Culicoides kingi, Austen: A vector of Onchocerca gutturosa (Neumann, 1910) in the Sudan. Ann. Trop. Med. Parasitol. 1980; 74: 655–656.
10. Scott DM, Griffin WHCE. Skin immune system and allergic skin diseases. In: Saunders W. (Ed.), Small Animal Dermatology. 2001; 543–666.
11. Schaffartzika A, Hamzab E, Jandab J, Crameria R, Martib E, Rhyner C. Equine insect bite hypersensitivity: What do we know? Veterinary Immunology and Immunopathology. 2012; 147: 113– 126.
12. Crilly JP, Nuttall T, del Pozo J, Hopker A, Tomlinson M, Sargison N. Hypersensitivity to Culicoides midges causing seasonal dermatitis in sheep. Veterinary Parasitology: Regional Studies and Reports. 2016; 3–4: 53–56. doi: 10.1016/j.vprsr.2016.06.001
13. Slama D, Haouas N, Mezhoud H, Babba H, Chaker E. Blood meal analysis of Culicoides (Diptera: Ceratopogonidae) in central Tunisia. PLoS One. 2015; 10 (3): doi.org/10.1371/journal.pone.0120528.
14. Keesing F, Holt RD, Ostfeld RS. Effects of species diversity on disease risk. Ecol Lett. 2006; 9: 485–498.
15. Goffredo M, Meiswinkel R. Entomological surveillance of bluetongue in Italy: methods of capture, catch analysis and identification of Culicoides biting midges. Vet. Ital. 2004; 40: 260–265.
16. Delécolle J.-C.: Nouvelle contribution à l’étude systematique et iconographique des espèces du genre Culicoides (Diptera: Ceratopogonidae) du nord-est de la France. Université Louis Pasteur de Strasbourg. 1985.
17. Mathieu B, Cetre-Sossah C, Garros C, Chavernac D, Balenghien T, Carpenter S, Setier-Rio ML, Vignes-Lebbe R, Ung V, Candolfi E, Delécolle JC. Development and validation of IIKC: an interactive identification key for Culicoides (Diptera: Ceratopogonidae) females from the Western Palaearctic region. Parasites & Vectors, 2012; 5, 137.
18. Dyce AL. The recognition of nulliparous and parous Culicoides (Diptera: Ceratopogidae) without dissection. Journal of the Australian Entomology Society. 1969; 8:11–15.
19. Rádrová J, Seblová V, Votýpka J. Feeding behavior and spatial distribution of Culex mosquitoes (Diptera: Culicidae) in wetland areas of the Czech Republic. Journal Medical Entomology. 2013; 50, 1097–104.
20. Adler PH, Tuten HC, Nelder MP. Arthropods of medico veterinary importance in zoos. Annu Rev Entomol. 2011; 56:123–142.
21. Puente MJ, Ruiz S, Soriguer R, Figuerola J. Effect of blood meal digestion and DNA extraction protocol on the success of blood meal source determination in the malaria vector Anopheles atroparvus. Malaria journal. 2013; 12(1): 109.
22. Sandres CJ, Shortall CR, Gubbins S, Burgin L, Gloster J, Harrington R, Reynolds D, Mellor P, Carpenter S. Influence of season and meteorological parameters on flight activity of Culicoides biting midges. Journal of Applied Ecology. 2011; 48: 1355–1364.
23. Bursell E. Enviromental aspects: Humidity. Rockstein, ed. Physiology of the Insecta. Academic Press, New York. 1964; 324–358.
24. Valkiúnas G. Avian malaria parasites and other haemosporidia. CRC PRESS. 2004; 946 pp. ISBN: 9780415300971
25. Synek P, Munciinger P, Albrecht T, Votýpka J. Avian haemosporidians in haematophagous insects in the Czech Republic. Parasitol Res. 2013; 112: 839–845.
26. Alarcon S D, Havelka P, Pineda E, Segelbacher G, Schaefer M. Urban forests as hubs for novel zoonosis: blood meal analysis, seasonal variation in Culicoides (Diptera: Ceratopogonidae) vectors, and avian haemosporidians. Parasitology. 2013; 140 (14): 1799–810. doi: 10.1017/S0031182013001285.
27. Bobeva A, Zehtindjiev P, Ilieva M, Dimitrov D, Mathis A, Bensch S. Host preferences of ornithophilic biting midges of the genus Culicoides in the Eastern Balkans. Medical and Veterinary Entomology. 2015; 29, 290–296.
28. Nelder PM, Swanson AD, Adler PH, Grogan LW. Biting midges of the genus Culicoides in South Carolina zoos. J Insect Sci. 2010; 10, 55. doi: 10.1673/031.010.5501
29. Sarvašová A, Kočišová A, Candolfi E, Mathieu B. Description of Culicoides (Culicoides) bysta n. sp., a new member of the Pulicaris group (Diptera: Ceratopogonidae) from Slovakia. Parasites & Vectors. 2017; 10, 279.
30. Englad EM, Pearce-Kelly P, Brugman AV, King S, Gubbins S, Sach F, Sanders JCH, Masters JN, Denison E, Carpenter S. Culicoides species composition and molecular identification of host blood meals at two zoos in the UK. Parasites & Vectors. 2020; 13, 139. doi.org/10.1186/s13071-020-04018-0
31. Beaver PC, Horner GS, Bilos JZ. Zoonotic onchocercosis in a resident of Illinois and observations on the identification of Onchocerca species. Am J Trop Med Hyg. 1974; 23, 595–607.
32. Koehsler M, Soleiman A, Aspöck H, Auer H, Walochnik J. Onchocerca jakutensis filariasis in humans. Emerg Infect Dis. 2007; 13,1749–52.
33. Orihel TC, Eberhard ML. Zoonotic filariasis. Clin. Microbiol. Rev. 1998; 11, 366–381.
34. Pampiglione S, Vakalis N, Lyssimachou A, Kouppari G, Orithel TC. Subconjunctival zoonotic Onchocerca in an Albanian man. Ann Trop Med Parasitol. 2001; 95, 827–832.
35. Sallo F, Eberhard ML, Fok E, Baska F, Hatvani I. Zoonotic intravitreal Onchocerca in Hungary. Ophthalmology. 2005; 112, 502–504.
36. Wesołowska M, Zając‑Pytrus H, Masny A, Pytrus W, Knysz B, Golab E, Sałamatin R. Onchocerca jakutensis ocular infection in Poland: a new vector‑borne human health risk? Parasites & Vectors. 2020; 13, 61. doi.org/10.1186/s13071-020-3925-6
37. Wright RW, McLean M, Neafie RC, Markman AW. Zoonotic onchocerciasis of the shoulder: A case report. The Journal of Bone and Joint Surgery. 2002; 84, 627-629.
38. Cambra-Pellejà M, Gandasegui J, Balaña-Fouce R, Muñoz J, Martínez-Valladares M. Zoonotic implications of Onchocerca species on human health. Pathogens. 2020; 9, 761. doi:10.3390/pathogens9090761
39. Stavrou A, Daly JM, Maddison B, Gough K, Tarlinton R. How is Europe positioned for a re-emergence of Schmallenberg virus? Veterinary Journal. 2017; 230, 45–51.