Parasites, Hosts and Diseases

The Korea Society for Parasitology and Tropical Medicine (대한기생충학·열대의학회)
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Asia and Europe: So Distant So Close? The Case of Lipoptena fortisetosa in Italy

  • Andreani, Annalisa (Department of Agriculture, Food, Environment and Forestry (DAGRI), University of Florence) ;
  • Giangaspero, Annunziata (Department of Agriculture, Food, Natural Resources and Engineering (DAFNE), University of Foggia) ;
  • Marangi, Marianna (Department of Agriculture, Food, Natural Resources and Engineering (DAFNE), University of Foggia) ;
  • Barlaam, Alessandra (Department of Agriculture, Food, Natural Resources and Engineering (DAFNE), University of Foggia) ;
  • Ponzetta, Maria Paola (Department of Agriculture, Food, Environment and Forestry (DAGRI), University of Florence) ;
  • Roy, Lise (CEFE, Univ Montpellier, CNRS, EPHE, IRD, Univ Paul) ;
  • Belcari, Antonio (Department of Agriculture, Food, Environment and Forestry (DAGRI), University of Florence) ;
  • Sacchetti, Patrizia (Department of Agriculture, Food, Environment and Forestry (DAGRI), University of Florence)
  • Received : 2020.08.02
  • Accepted : 2020.10.13
  • Published : 2020.12.31
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Abstract

In Europe, 5 Lipoptena species have been recorded, including Lipoptena fortisetosa. This species, native to Asian countries, was described as a parasite of sika deer and its appearance in Europe dates back to more than 50 years ago. Lipoptena fortisetosa has been recently reported in Italy, sharing its hosts with Lipoptena cervi. A morpho-molecular approach was developed to determine the phylogenetic interrelationship of Italian and Asian CO1 haplotypes sequenced from Lipoptena fly individuals collected in Italy, and their DNA sequences were compared with conspecifics available in GenBank; morphological key-characters (terminalia) of L. fortisetosa were compared with the original description. Two haplotypes were recorded from Italy and assigned to L. cervi and L. fortisetosa, respectively. The latter was part of the monophyletic clade L. fortisetosa, along with 2 Central European and 2 Korean haplotypes (100% identical to one of the Korean haplotypes); moreover, Italian L. fortisetosa female terminalia were consistent with the original description of Asian individuals. Pending more in-depth investigations, this study provides a first answer to the hypothesis of the recent colonization of Italy by L. fortisetosa from Asia as we did not detect any obvious and stable morphological and molecular differences in specimens from the 2 geographical areas. The presence of the sika deer in Europe was retraced and the possible route traveled by the parasite from Asia and the eco-biological factors that may have enhanced its settlement are discussed.

Keywords

References

  1. Dick CW. Checklist of world Hippoboscidae (Diptera: Hippoboscoidea). Chicago, USA. Department of Zoology, Field Museum of Natural History. 2006, pp 1-7.
  2. Kortet R, Harkonen L, Hokkanen P, Harkonen S, Kaitala A, Kaunisto S, Laaksonen S, Kekalainen J, Ylonen H. Experiments on the ectoparasitic deer ked that often attacks humans; preferences for body parts, colour and temperature. Bull Entomol Res 2010; 100: 279-285. https://doi.org/10.1017/S0007485309990277
  3. Soos A, Hurka K. Family hippoboscidae. In Soos A, Papp L eds, Catalogue of Palaearctic Diptera, Vol 11. Budapest, Hungary. Akademiai Kaido 1986, pp 215-226.
  4. Skvarla MJ, Machtinger ET. Deer keds (Diptera: Hippoboscidae: Lipoptena and Neolipoptena) in the United States and Canada: new state and county records, pathogen records, and an illustrated key to species. J Med Entomol 2019; 56: 744-760. https://doi.org/10.1093/jme/tjy238
  5. GBIF.org. GBIF Home Page [Internet]; [cited 2020 September 20]. Available from: https://www.gbif.org
  6. Visagie EJ. A new species of Lipoptena (Diptera: Hippoboscidae) from Southern Africa. Onderstepoort J Vet Res 1992; 59: 293-302.
  7. Harkonen S, Laine M, Vornanen M, Reunala T. Deer ked (Lipoptena cervi) dermatitis in humans-an increasing nuisance in Finland. Alces 2009; 45: 73-79.
  8. Lazar M, Iacob OC, Solcan C, Pasca SA, Lazar R, Boisteanu PC. The first report of massive infestation with Lipoptena cervi (Diptera: Hippoboscidae) in roe deer (Capreolus capreolus) in Iasi county, N-E of Romania. Arq Bras Med Vet Zootec 2017; 69: 293-298. https://doi.org/10.1590/1678-4162-8612
  9. Salvetti M, Bianchi A, Marangi M, Barlaam M, Giacomelli S, Bertoletti I, Roy L, Giangaspero A. Deer keds on wild ungulates in northern Italy, with a taxonomic key for the identification of Lipoptena spp. of Europe. Med Vet Entomol 2020; 34: 74-85. https://doi.org/10.1111/mve.12411
  10. Gothe R, Schol H. Deer keds (Lipoptena cervi) in the accompanying equipment of the late Neolithic human mummy from the Similaun, South Tyrol. Parasitol Res 1994; 80: 81-83. https://doi.org/10.1007/BF00932630
  11. Fauna Europaea. All European Animal Species Online [Internet]; [cited 2020 September 20]. Available from: https://fauna-eu.org.
  12. Dehio C, Sauder U, Hiestand R. Isolation of Bartonella schoenbuchensis from Lipoptena cervi, a blood-sucking arthropod causing deer ked dermatitis. J Clin Microbiol 2004; 42: 5320-5323. https://doi.org/10.1128/JCM.42.11.5320-5323.2004
  13. Duodu S, Madslien K, Hjelm E, Molin Y, Paziewska-Harris A, Harris PD, Colquhoun DJ, Ytrehus B. Bartonella infections in deer Keds (Lipoptena cervi) and moose (Alces alces) in Norway. Appl Environ Microbiol 2013; 79: 322-327. https://doi.org/10.1128/AEM.02632-12
  14. Szewczyk T, Werszko J, Steiner-Bogdaszewska Z, Jezewski W, Laskowski Z, Karbowiak G. Molecular detection of Bartonella spp. in deer ked (Lipoptena cervi) in Poland. Parasit Vectors 2017; 10: 487. https://doi.org/10.1186/s13071-017-2413-0
  15. Chomel BB, Boulouis HJ, Breitschwerdt EB, Kasten RW, VayssierTaussat M, Birtles RJ, Koehler JE, Dehio C. Ecological fitness and strategies of adaptation of Bartonella species to their hosts and vectors. Vet Res 2009; 40: 29. https://doi.org/10.1051/vetres/2009011
  16. Hornok S, de la Fuente J, Biro N, Fernandez de Mera IG, Meli ML, Elek V, Gonczi E, Meili T, Tanczos B, Farkas R, Lutz H, Hofmann-Lehmann R. First molecular evidence of Anaplasma ovis and Rickettsia spp. in keds (Diptera: Hippoboscidae) of sheep and wild ruminants. Vector Borne Zoonotic Dis 2011; 11: 1319-1321. https://doi.org/10.1089/vbz.2011.0649
  17. Kelsey A, Finch J. Deer ked: a Lyme-carrying ectoparasite on the move. Cutis 2018; 102: 121-122.
  18. Maa TC. A synopsis of the Lipopteninae (Diptera: Hippoboscidae). J Med Entomol 1965; 2: 233-248. https://doi.org/10.1093/jmedent/2.3.233
  19. Maa TC. A revised checklist and concise host index of Hippoboscidae (Diptera). Pacific Insects Monograph 1969; 20: 261-269.
  20. Mogi M. A new species of Lipoptena (Diptera, Hippoboscidae) from the Japanese deer. Kontyu 1975; 43: 387-392.
  21. Yamauchi T, Tsurumi M, Kataoka N. Distributional records of Lipoptena species (Diptera: Hippoboscidae) in Japan and Jeju-do, Korea. Med Entomol Zoo 2009; 60: 131-133. https://doi.org/10.7601/mez.60.131
  22. Choi CY, Lee S, Moon KH, Kang CW, Yun YM. New Record of Lipoptena fortisetosa (Diptera: Hippoboscidae) collected from Siberian roe deer on Jeju Island, Korea. J Med Entomol 2013; 50: 1173-1177. https://doi.org/10.1603/me12150
  23. Edwards SJ, Hood MW, Shaw JH, Rayburn JD, Kirby MD, Hanfman DT, Zidar JA. Index-Catalogue of Medical and Veterinary Zoology. Supplement 21, Part 5: Parasite-Subject Catalogue. Parasites: Arthropoda and Miscellaneous Phyla. Washington DC, USA. USDA Government Printing Office. 1978, pp 246.
  24. Theodor O. Lipoptena parvula, n. sp., eine neue Art aus der Tschechoslowakei (Diptera, Hippoboscidae). Acta Entomol Mus Natl Pragae 1965; 37: 275-278.
  25. Grunin KJ. Hippoboscidae-krovososki. In Bej-Bienko GJ ed. Opredlitl nasekomych evropejskoj czasti SSSR. T. 5. Nauka, Leningrad. 1970, pp 979-987 (in Russian).
  26. Kurina O, Kirik H, Ounap H, Ounap E. The northernmost record of a blood-sucking ectoparasite, Lipoptena fortisetosa Maa (Diptera: Hippoboscidae), in Estonia. Biodivers Data J 2019; 7: e47857. https://doi.org/10.3897/BDJ.7.e47857
  27. Andreani A, Belcari A, Sacchetti P, Ponzetta MP. Occurrence of a new parasite of the ungulates in Italy: Lipoptena fortisetosa (Diptera: Hippoboscidae). Atti del IV Congresso Nazionale di Ecopatologia della Fauna ; 2017 October 11-13. S.I.E.F. Società Italiana di Ecopatologia della Fauna. 2017, pp 36.
  28. Andreani A, Sacchetti P, Belcari A. Comparative morphology of the deer ked Lipoptena fortisetosa first recorded from Italy. Med Vet Entomol 2019; 33: 140-153. https://doi.org/10.1111/mve.12342
  29. Buttiker W. Die Lausfliegen der Schweitz (Diptera, Hippoboscidae): mit Bestimmungsschlüssel. Neuchatel, Switzerland. Centre Suisse de cartographie de la faune. 1994, pp 1-117 (in German).
  30. Schedl W. Beitrag zur Lausfliegen-Fauna an Saugetieren von Karnten und anderen Bundeslandern Österreichs (Insecta: Diptera, Hippoboscidae). Linzer biol Beitr 2018; 50: 1283-1293 (in Deutsch).
  31. Metelitsa AK, Veselkin GA. Parasitism of the louse fly Lipoptena fortisetosa on cattle. Parazitologiia 1989; 23: 276-277. [In Russian].
  32. Sokol R. Galecki R. Prevalence of keds on city dogs in Central Poland. Med Vet Entomol 2017; 31: 114-116. https://doi.org/10.1111/mve.12209
  33. Mihalca AD, Pastrav IR, Sandor AD, Deak G, Gherman CM, Sarmasi A, Votypka J. First report of the dog louse fly Hippobosca longipennis in Romania. Med Vet Entomol 2019; 33: 530-535. https://doi.org/10.1111/mve.12395
  34. Schumann H, Messner B. Erstnachweis von Lipoptena fortisetosa Maa, 1965 in Deutschland (Dipt., Hippoboscidae). Entomol Nachr Ber 1993; 37: 247-249.
  35. Obona J, Sychra O, Gres S, Herman P, Manko P, Rohacek J, Sestakova A, Slapak J, Hromada M. A revised annotated checklist of louse flies (Diptera, Hippoboscidae) from Slovakia. ZooKeys 2019; 862: 129-152. https://doi.org/10.3897/zookeys.862.25992
  36. Lee SH, Kim KT, Kwon OD, Ock Y, Kim T, Choi D, Kwak D. Novel detection of Coxiella spp., Theileria luwenshuni, and T. ovis endosymbionts in deer keds (Lipoptena fortisetosa). PLoS One 2016; 11: e0156727. https://doi.org/10.1371/journal.pone.0156727
  37. Werszko J, Steiner-Bogdaszewska Z, Jezewski W, Szewczyk T, Kurylo G, Wolkowycki M, Wroblewski P, Karbowiak G. Molecular detection of Trypanosoma spp. in Lipoptena cervi and Lipoptena fortisetosa (Diptera: Hippoboscidae) and their potential role in the transmission of pathogens. Parasitology. 2020; 1-26. https://doi.org/10.1017/S0031182020001584.
  38. Kowal J, Nosal P, Kornas S, Wajdzik M, Matysek M, Basiaga M. Biodiversity and importance of hippoboscids infection in cervids. Med Weter 2016; 72: 745-749.
  39. Schlick-Steiner BC, Steiner FM, Seifert B, Stauffer C, Christian E, Crozier RH. Integrative taxonomy: a multisource approach to exploring biodiversity. Annu Rev Entomol 2010; 55: 421-438. https://doi.org/10.1146/annurev-ento-112408-085432
  40. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R. DNA primers for amplification of mitochondrial cytochrome CO1idase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 1994; 3: 294-299.
  41. Maa T.C., Peterson BV. Hippoboscidae. In McAlpine JF, Peterson BV, Shewell GE, Teskey HJ, Vockeroth JR, Wood DM eds, Manual of Nearctic Diptera, Vol. II. Monograph 28. Ottawa, ON, Canada. Research Branch, Agriculture Canada. 1987; pp 1271-1281.
  42. McAlpine JF. Morphology and terminology - Adults. In McAlpine JF, Peterson BV, Shewell GE, Teskey HJ, Vockeroth JR, Wood DM eds, Manual of Nearctic Diptera, Vol. I. Monograph 27. Ottawa, ON, Canada. Research Branch, Agriculture Canada. 1981; pp 9-63.
  43. Bequaert J. A monograph of the Melophaginae, or ked-flies, of sheep, goats, deer and antelopes (Diptera, Hippoboscidae). Entomol Americana 1942; 22: 1-220.
  44. Bartos L. Sika deer in continental Europe. In McCullough DR, Takatsuki S, Kaji K eds, Sika Deer: Biology and Management of Native and Introduced Populations. Tokyo, Japan. Springer. 2009, pp 573-594.
  45. Lowe VPW, Gardiner AS. Hybridization between Red deer (Cervus elaphus) and Sika deer (Cervus nippon) with particular reference to stocks in N.W. England. J Zool 1975; 177: 553-566. https://doi.org/10.1111/j.1469-7998.1975.tb02259.x
  46. Goodman SJ, Barton NH, Swanson G, Abernethy K, Pemberton JM. Introgression through rare hybridization: a genetic study of a hybrid zone between Red and Sika deer (Genus Cervus) in Argyll, Scotland. Genetics 1999; 152: 355-371. https://doi.org/10.1093/genetics/152.1.355
  47. Carden RF, Carlin CM, Marnell F, Mcelholm D, Hetherington J, Gammell MP. Distribution and range expansion of deer in Ireland. Mammal Rev 2011; 41: 313-325. https://doi.org/10.1111/j.1365-2907.2010.00170.x
  48. Biedrzycka A, Solarz W, Okarma H. Hybridization between native and introduced species of deer in Eastern Europe. J Mammal 2012; 93: 1331-1341. https://doi.org/10.1644/11-MAMM-A-022.1
  49. Ferri M, Fontana R, Lanzi A, Armaroli E, Peloso F, Musarò C, Andina L, Allegri M, Adorni PL, Gelmini L, Barancekovà M, Levrini M, De Pietri A, Berti E. Some Sika deer (Cervus nippon) recently hunted and spotted free-ranging in the Emilia-Romagna's region (and out of it) question the management of Italian Red deer (Cervus elaphus) population. X Congresso Italiano di Teriologia, Hystrix 2016; 27 (suppl): 100.
  50. Raganella Pelliccioni E, Riga F, Toso S. Linee Guida per la gestione degli Ungulati: Cervidi e Bovidi. Roma, Italy. ISPRA Press. 2013, pp 1-220 (in Italiano)
  51. Kim H, Hoelmer KA, Lee W, Kwon YD, Lee S. Molecular and morphological identification of the soybean aphid and other aphis species on the primary host Rhamnus davurica in Asia. Ann Entomol Soc Am 2010; 103: 532-543. https://doi.org/10.1603/AN09166
  52. Hendrichs J, Vera T, De Meyer M, Clarke AR. Resolving cryptic species complexes of major tephritid pests. Zookeys 2015; 540: 5-39. https://doi.org/10.3897/zookeys.540.9656

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