Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-28T15:13:01.278Z Has data issue: false hasContentIssue false
  • English
  • Français

Ectoparasites of red foxes (Vulpes vulpes) with a particular focus on ticks in subcutaneous tissues

Published online by Cambridge University Press:  14 July 2020

Dorota Dwużnik Open the ORCID record for Dorota Dwużnik [Opens in a new window] ,
Ewa Julia Mierzejewska ,
Maciej Kowalec ,
Mohammed Alsarraf Open the ORCID record for Mohammed Alsarraf [Opens in a new window] ,
Łukasz Stańczak ,
Patrycja Opalińska ,
Małgorzata Krokowska-Paluszak Open the ORCID record for Małgorzata Krokowska-Paluszak [Opens in a new window] ,
Grzegorz Górecki  and
Anna Bajer Open the ORCID record for Anna Bajer [Opens in a new window]
Dorota Dwużnik*
Affiliation:
Department of Eco-Epidemiology of Parasitic Diseases, Institute of Developmental Biology and Biomedical Sciences, Faculty of Biology, University of Warsaw, Miecznikowa 1, 02-096 Warsaw, Poland
Ewa Julia Mierzejewska
Affiliation:
Department of Eco-Epidemiology of Parasitic Diseases, Institute of Developmental Biology and Biomedical Sciences, Faculty of Biology, University of Warsaw, Miecznikowa 1, 02-096 Warsaw, Poland
Maciej Kowalec
Affiliation:
Department of Eco-Epidemiology of Parasitic Diseases, Institute of Developmental Biology and Biomedical Sciences, Faculty of Biology, University of Warsaw, Miecznikowa 1, 02-096 Warsaw, Poland
Mohammed Alsarraf
Affiliation:
Department of Eco-Epidemiology of Parasitic Diseases, Institute of Developmental Biology and Biomedical Sciences, Faculty of Biology, University of Warsaw, Miecznikowa 1, 02-096 Warsaw, Poland
Łukasz Stańczak
Affiliation:
Department of Game Management and Forest Protection, Poznań University of Life Sciences, Wojska Polskiego 71d, 60-625 Poznań, Poland
Patrycja Opalińska
Affiliation:
Department of Game Management and Forest Protection, Poznań University of Life Sciences, Wojska Polskiego 71d, 60-625 Poznań, Poland
Małgorzata Krokowska-Paluszak
Affiliation:
Department of Game Management and Forest Protection, Poznań University of Life Sciences, Wojska Polskiego 71d, 60-625 Poznań, Poland
Grzegorz Górecki
Affiliation:
Department of Game Management and Forest Protection, Poznań University of Life Sciences, Wojska Polskiego 71d, 60-625 Poznań, Poland
Anna Bajer
Affiliation:
Department of Eco-Epidemiology of Parasitic Diseases, Institute of Developmental Biology and Biomedical Sciences, Faculty of Biology, University of Warsaw, Miecznikowa 1, 02-096 Warsaw, Poland
*
Author for correspondence: Dorota Dwużnik, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

In the present study, we identified the ectoparasite communities of red foxes in three regions of Poland that encompassed two endemic regions for the occurrence of Dermacentor reticulatus, as well as a region that is free of this tick species (‘gap’ area). Our study sites were selected to enable the role of foxes as hosts for juvenile (nest dwelling) and adult (exophilic) D. reticulatus ticks to be determined, and to assess their contribution to the spread of this important vector of Babesia canis. We compared also ectoparasite communities between adult foxes with those of fox cubs. Finally, we carried out a systematic search for subcutaneous ticks determining their prevalence and abundance. In 2016–2018, 366 adult foxes and 25 live-trapped cubs were examined for ectoparasites. Ectoparasites were identified based on morphological features, PCR amplification and sequencing. The total prevalence of ectoparasites was higher in cubs (68%) than in adults (62.8%). In adults, 15 parasite species were recorded, including four tick species, seven flea species, scabies, and one Anopluran species each in the genera Felicola and Lipoptena. In cubs, six ectoparasite species were found, including Ixodes kaiseri, a species not found in adults. Although Ixodes ricinus and D. reticulatus were the dominant tick species on adult foxes, no D. reticulatus ticks were found on cubs. Subcutaneous ticks were common (38%) and abundant in all areas. Molecular analysis of subcutaneous nodules allowed the identification of 17 I. ricinus and five D. reticulatus. In conclusion, red foxes play a minor role as hosts of D. reticulatus.

Keywords

Dermacentor reticulatusectoparasites communityfleasIxodes canisugaIxodes hexagonusIxodes kaiseriIxodes ricinussubcutaneous ticks
Type
Research Article
Information
Parasitology , Volume 147 , Issue 12 , October 2020 , pp. 1359 - 1368
Check for updates
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adkins, CA and Stott, P (1998) Home ranges, movements and habitat associations of red foxes Vulpes vulpes in suburban Toronto, Ontario, Canada. Journal of Zoology 244, 335–346.CrossRefGoogle Scholar
Bajer, A, Mierzejewska, EJ, Rodo, A, Bednarska, M, Kowalec, M and Welc-Falęciak, R (2014a) The risk of vector-borne infections in sled dogs associated with existing and new endemic areas in Poland: Part 1: a population study on sled dogs during the racing season. Veterinary Parasitology 202, 276–286. http://dxdoiorg/101016/jvetpar201312033.CrossRefGoogle Scholar
Bajer, A, Mierzejewska, EJ, Rodo, A and Welc-Falęciak, R (2014b) The risk of vector-borne infections in sled dogs associated with existing and new endemic areas in Poland: Part 2: occurrence and control of babesiosis in a sled dog kennel during a 13-year-long period. Veterinary Parasitology 202, 234–240.CrossRefGoogle Scholar
Bajer, A, Rodo, A, Alsarraf, M, Dwuznik, D, Behnke, JM and Mierzejewska, EJ (2017) Abundance of the tick, Dermacentor reticulatus, in an ecosystem of abandoned meadows: experimental intervention and the critical importance of mowing. Veterinary Parasitology 246, 70–75.CrossRefGoogle Scholar
Buckle, A and Harris, S (1980) The flea epifauna of a suburban fox (Vulpes vulpes) population. Journal of Zoology 190, 431–439.CrossRefGoogle Scholar
Carricondo-Sanchez, D, Odden, M, Linnell, JDC and Odden, J (2017) The range of the mange: spatiotemporal patterns of sarcoptic mange in red foxes (Vulpes vulpes) as revealed by camera trapping. PLoS ONE 12, e0176200.CrossRefGoogle ScholarPubMed
Cavallini, P (1996) Ranging behaviour of red foxes during the mating and breeding seasons. Ethology Ecology & Evolution 8, 57–65 DOI: 101080/0892701419969522935.CrossRefGoogle Scholar
Chang, SH, Park, JH, Kwak, JE, Joo, M, Kim, H, Chi, JG, Hong, ST and Chai, JY (2006) A case of histologically diagnosed tick infestation on the scalp of a Korean child Korean. Journal of Parasitology 44, 157–161.Google ScholarPubMed
Checa, R, López-Beceiro, AM, Montoya, A, Barrera, JP, Ortega, N, Gálvez, R, Marino, V, González, J, Olmeda, AS, Fidalgo, LU and Miró, G (2018) Babesia microti-like piroplasm (syn. Babesia vulpes) infection in red foxes (Vulpes vulpes) in NW Spain (Galicia) and its relationship with Ixodes hexagonus. Veterinary Parasitology 252, 22–28.CrossRefGoogle ScholarPubMed
D'Amico, G, Juránkoá, J, Tăbăran, FA, Frgelecová, L, Forejtek, P, Matei, IA, Ionică, AM, Hodžić, A, Modrý, D and Mihalca, AD (2017) Occurrence of ticks in the subcutaneous tissue of red Vulpes vulpes in Czech Republic and Romania. Ticks and Tick Borne Diseases 8, 309–312.CrossRefGoogle ScholarPubMed
Domínguez-Peñafiel, G, Giménez-Pardo, C, Gegúndez, MI and Lledó, L (2011) Prevalence of ectoparasitic arthropods on wild animals and cattle in the Las Merindades area (Burgos, Spain). Parasite 18, 251–260.CrossRefGoogle Scholar
Duscher, GG, Leschnik, M, Fuehrer, HP and Joachim, A (2015) Wildlife reservoirs for vector-borne canine, feline and zoonotic infections in Austria. International Journal for Parasitology. Parasites and wildlife 4, 88–96.CrossRefGoogle ScholarPubMed
Dwużnik, D, Mierzejewska, EJ, Drabik, P, Kloch, A, Alsarraf, M, Behnke, JM and Bajer, A (2019) The role of juvenile Dermacentor reticulatus ticks as vectors of microorganisms and the problem of ‘meal contamination’. Experimental and Applied Acarology 78, 181–202.CrossRefGoogle ScholarPubMed
Estrada-Peña, A, Nava, S and Petney, T (2014) Description of all the stages of Ixodes inopinatus sp. (Acari: Ixodidae). Ticks and Tick-Borne Diseases 5, 734CrossRefGoogle Scholar
Foley, P, Foley, J, Sándor, AD, Ionica, AM, Matei, IA, D'Amico, G, Gherman, CM, Doms, C and Mihalca, AD (2017) Diversity of flea (Siphonaptera) parasites on red foxes (Vulpes vulpes) in Romania. Journal of Medical Entomology 54, 1243–1250.CrossRefGoogle Scholar
Galloway, TD (2005) Ectoparasites from native and introduced birds from Christchurch and surrounding areas, New Zealand. Tuhinga 16, 13–20.Google Scholar
Goszczyński, J, Misiorowska, M and Juszko, S (2008) Changes in the density and spatial distribution of red fox dens and cub numbers in central Poland following rabies vaccination. Acta Theriologica 53, 121–127.CrossRefGoogle Scholar
Harris, S and Thompson, GB (1978) Populations of the ticks Ixodes (Pholeoixodes) hexagonus and Ixodes (Pholeoixodes) canisuga infesting suburban foxes, Vulpes vulpes. Journal of Zoology 186, 83–93.CrossRefGoogle Scholar
Hornok, S, Sándor, AD, Beck, R, Farkas, R, Beati, L, Kontschán, J, Takács, N, Földvári, G, Silaghi, C, Meyer-Kayser, E, Hodžić, A, Tomanović, S, Abdullah, S, Wall, R, Estrada-Peña, A, Duscher, GG and Plantard, O (2017) Contributions to the phylogeny of Ixodes (Pholeoixodes) canisuga, I. (Ph) kaiseri, I. (Ph) hexagonus and a simple pictorial key for the identification of their females. Parasites & Vectors 10, 545.CrossRefGoogle Scholar
Jongejan, F, Ringenier, M, Putting, M, Berger, L, Burgers, S, Kortekaas, R, Lenssen, J, Roessel, M, Wijnveld, M and Madder, M (2015) Novel foci of Dermacentor reticulatus ticks infected with Babesia canis and Babesia caballi in the Netherlands and in Belgium. Parasites & Vectors 8:232.CrossRefGoogle ScholarPubMed
Karbowiak, G, Szewczyk, T and Werszko, J (2016) Ectoparasites of carnivores in north-eastern Poland. Annals of Parasitology 62 (suppl.), 184.Google Scholar
Kiewra, D, Czułowska, A and Lonc, E (2016) Winter activity of Dermacentor reticulatus (Fabricius, 1794) in the newly emerging population of Lower Silesia, south-west Poland. Ticks and Tick-Borne Diseases 7, 1124–1127.CrossRefGoogle ScholarPubMed
Kočišová, A, Lazar, P and Letko, V (2006) Ectoparasitic species from red foxes (Vulpes vulpes) in East Slovakia. Veterinarski Arhiv 76, 599–563.Google Scholar
Kowalec, M, Szewczyk, T, Welc-Falęciak, R, Siński, E, Karbowiak, G and Bajer, A (2017) Ticks and the city – are there any differences between city parks and natural forests in terms of tick abundance and prevalence of spirochaetes? Parasites & Vectors 10, 573.CrossRefGoogle ScholarPubMed
Kulakova, NV, Khasnatinov, MA, Sidorova, EA, Adel`shin, RV and Belikov, SI (2014) Molecular identification and phylogeny of Dermacentor nuttalli (Acari: Ixodidae). Parasitology Research 113, 1787–1793.CrossRefGoogle Scholar
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: molecular evolutionary genetics analysis version 70 for bigger datasets. Molecular Biology and Evolution 3, 1870–1874.CrossRefGoogle Scholar
Meyer-Kayser, E, Hoffmann, L, Silaghi, C, Pfister, K, Mahling, M and Passos, LM (2012) Dynamics of tick infestations in foxes in Thuringia, Germany. Ticks and Tick-Borne Diseases 3, 232–239.CrossRefGoogle ScholarPubMed
Mierzejewska, EJ, Pawełczyk, A, Radkowski, M, Welc-Falęciak, R and Bajer, A (2015) Pathogens vectored by the tick, Dermacentor reticulatus, in endemic regions and zones of expansion in Poland. Parasites & Vectors 8, 490.CrossRefGoogle ScholarPubMed
Mierzejewska, EJ, Estrada-Peña, A, Alsarraf, M, Kowalec, M and Bajer, A (2016) Mapping of Dermacentor reticulatus expansion in Poland in 2012–2014. Ticks and Tick Borne Diseases 7, 94–106.CrossRefGoogle ScholarPubMed
Mierzejewska, EJ, Dwużnik, D, Tołkacz, K, Bajer, A, Panek, M and Grzybek, M (2020) The efficiency of live-capture traps for the study of red fox (Vulpes vulpes) cubs: A three-year study in Poland. Animals 10, 374. doi: 10.3390/ani10030374CrossRefGoogle Scholar
Mihalca, AD, Dumitrache, MO, Sándor, AD, Magdaş, C, Oltean, M, Györke, A, Matei, IA, Ionică, A, D'Amico, G, Cozma, V and Gherman, CM (2012) Tick parasites of rodents in Romania: host preferences, community structure and geographical distribution. Parasites & Vectors 5:266.CrossRefGoogle ScholarPubMed
Nei, M and Kumar, S (2000) Molecular Evolution and Phylogenetics. Oxford, US: Oxford University Press.Google Scholar
Nosek, J and Sixl, W (1972) Central-European ticks (Ixodoidea) key for determination.Google Scholar
Nutall, GH (1914) Penetration of Ixodes beneath the skin. Parasitology 7, 258–259.CrossRefGoogle Scholar
Panek, M and Bresiński, W (2002) Red fox Vulpes vulpes density and habitat use in a rural area of western Poland in the end of 1990s, compared with the turn of 1970s. Acta Theriologica 4, 433–442.CrossRefGoogle Scholar
Pawełczyk, A, Bajer, A, Behnke, JM, Gilbert, FS and Siński, E (2004) Factors affecting the component community structure of haemoparasites in common voles (Microtus arvalis) from the Mazury Lake District region of Poland. Parasitology Research 92, 270–284.CrossRefGoogle ScholarPubMed
Paziewska, A, Zwolińska, L, Harris, PD, Bajer, A and Siński, E (2010) Utilisation of rodent species by larvae and nymphs of hard ticks (Ixodidae) in two habitats in NE Poland. Experimental and Applied Acarology 50, 79–91.CrossRefGoogle ScholarPubMed
Petney, TN, Pfäffle, MP, Jasmin, D and Skuballa, JD (2012) An annotated checklist of the ticks (Acari: Ixodida) of Germany. Systematic And Applied Acarology UK 17, 115–170.Google Scholar
Pfäffle, M, Littwin, N and Trevor, P (2015) Host preferences of immature Dermacentor reticulatus (Acari: Ixodidae) in a forest habitat in Germany. Ticks and Tick-Borne Diseases 6, 508–515. 101016/jttbdis201504003.CrossRefGoogle Scholar
Radzijevskaja, J, Mardosaitė-Busaitienė, D, Aleksandravičienė, A and Paulauskas, A (2018) Investigation of Babesia spp. in sympatric populations of Dermacentor reticulatus and Ixodes ricinus ticks in Lithuania and Latvia. Ticks and Tick-Borne Diseases 9, 270–274.CrossRefGoogle ScholarPubMed
Rubel, F, Brugger, K, Pfeffer, M, Chitimia-Dobler, L, Didyk, YM, Leverenz, S, Dautel, H and Kahl, O (2016) Geographical distribution of Dermacentor marginatus and Dermacentor reticulatus in Europe. Tick and Tick Borne Diseases 7, 224–233.CrossRefGoogle ScholarPubMed
Sándor, AD, D'Amico, G, Gherman, CM, Dumitrache, MO, Domșa, C and Mihalca, DA (2017) Mesocarnivores and macroparasites: altitude and land use predict the ticks occurring on red foxes (Vulpes vulpes). Parasites & Vectors 10:173.CrossRefGoogle Scholar
Skuratowicz, W (1967) Klucze do Oznaczania Owadów Polski; Część XXIX Pchły – Siphonaptera (Aphaniteptera). Opracowanie Zbiorowe. Warszawa, PL: Państwowe Wydawnictwo Naukowe, (In Polish).Google Scholar
Smith, DD, Frenkel, JK and Smith, EI (1986) Intradermal infestation of a red fox (Vulpes vulpes) by the lone star tick (Amblyomma americanum). Journal of Wildlife Diseases 22, 122–124.CrossRefGoogle Scholar
Sréter, T, Széll, Z and Varga, I (2003) Ectoparasite infestations of red foxes (Vulpes vulpes) in Hungary. Veterinary Parasitology 115, 349–354.CrossRefGoogle Scholar
Szymański, S (1986) Distribution of the tick Dermacentor reticulatus (Fabricius, 1794) (Ixodidae) in Poland. Acta Parasitologica Polonica 31, 143–154.Google Scholar
Trewhella, WJ, Harris, A and McAllister, FE (1989) Dispersal distance, home range size and population density in the red fox (Vulpes vulpes): a quantitative analysis. Journal of Applied Ecology 25, 423–434.CrossRefGoogle Scholar
Tugwell, P and Lancaster, JL (1962) Results of a tick-host study in northwest Arkansas. Journal of the Kansas Entomological Society 35, 202–211.Google Scholar
Víchová, B, Bona, M, Miterpáková, M, Kraljik, J, Čabanová, V, Nemčíková, G, Hurníková, Z and Oravec, M (2018) Fleas and ticks of red foxes as vectors of canine bacterial and parasitic pathogens, in Slovakia, Central Europe. Vector-Borne and Zoonotic Diseases 18, 611–619CrossRefGoogle ScholarPubMed
Wegner, Z (1972) Klucze do Oznaczania Owadów Polski; Część XVI Wszy – Anoplura. Opracowanie Zbiorowe. Warszawa, PL: Państwowe Wydawnictwo Naukowe, (In Polish).Google Scholar
Whitaker, J, Dick, C and Ritzi, C (2009) Collecting and preserving ectoparasites for ecological study. In Parsons, S and Kuntz, TH (eds), Ecological and Behavioral Methods for the Study of Bats. Baltimore, US: Johns Hopkins University Press, 806–882.Google Scholar
Wodecka, B, Michalik, J, Lane, RS, Nowak-Chmura, M and Wierzbicka, A (2016) Differential associations of Borrelia species with European badgers (Meles meles) and raccoon dogs (Nyctereutes procyonoides) in western Poland. Ticks and Tick-Borne Diseases 7, 1010–1016.CrossRefGoogle Scholar
Złotorzycka, J (1972) Klucze do Oznaczania Owadów Polski; Część XV Wszoły – Mallophga. Opracowanie Zbiorowe. Warszawa, PL: Państwowe Wydawnictwo Naukowe, (In Polish).Google Scholar