Abstract
So far, neither the feline lungworms Aelurostrongylus abstrusus and Troglostrongylus brevior nor the canine lungworm Angiostrongylus vasorum was reported in wildlife or intermediate hosts from Austria. The slug Arion vulgaris represents an invasive species in Europe and serves as intermediate host for several lungworm species. This study aimed to analyse the occurrence of metastrongyloid lungworm larvae in slugs in Vienna, Austria. Therefore, 193 A. vulgaris were collected in the central Prater park in summer 2016. Specimens were artificially digested, analysed microscopically for lungworm larvae, and species were confirmed via PCR and sequencing. Out of 193, five slugs were positive to lungworms (2.6%), one for A. vasorum, two for A. abstrusus (genotypes A and B) and one for T. brevior, and one slug had a mixed infection of A. abstrusus and T. brevior larvae. The current study is the first evidence on the endemicity of these metastrongyloid lungworm species in Austria.
References
Barutzki D, Dyachenko V, Schaper R (2017) Lungworms in Germany 2002–2016: is there an increase in occurrence and geographical spread? Parasitol Res 116:11–30. https://doi.org/10.1007/s00436-017-5488-9
Di Cesare A, Traversa D (2014) Canine angiostrongylosis: recent advances in diagnosis, prevention, and treatment. Vet Med 2014:181–192. https://doi.org/10.2147/VMRR.S53641
Di Cesare A, Frangipane di Regalbono A et al (2014) Mixed infection by Aelurostrongylus abstrusus and Troglostrongylus brevior in kittens from the same litter in Italy. Parasitol Res 113:613–618. https://doi.org/10.1007/s00436-013-3690-y
Dörler D, Kropf M, Laaha G, Zaller JG (2018) Occurrence of the invasive Spanish slug in gardens: can a citizen science approach help deciphering underlying factors? BMC Ecol 18:23. https://doi.org/10.1186/s12898-018-0179-7
Elsheikha HM, Schnyder M, Traversa D, di Cesare A, Wright I, Lacher DW (2016) Updates on feline aelurostrongylosis and research priorities for the next decade. Parasit Vectors 9:389. https://doi.org/10.1186/s13071-016-1671-6
Giannelli A, Capelli G, Joachim A, Hinney B, Losson B, Kirkova Z, René-Martellet M, Papadopoulos E, Farkas R, Napoli E, Brianti E, Tamponi C, Varcasia A, Margarida Alho A, Madeira de Carvalho L, Cardoso L, Maia C, Mircean V, Mihalca AD, Miró G, Schnyder M, Cantacessi C, Colella V, Cavalera MA, Latrofa MS, Annoscia G, Knaus M, Halos L, Beugnet F, Otranto D (2017) Lungworms and gastrointestinal parasites of domestic cats: a European perspective. Int J Parasitol 47:517–528. https://doi.org/10.1016/j.ijpara.2017.02.003
Gillis-Germitsch N, Kapel CMO, Thamsborg SM, Deplazes P, Schnyder M (2017) Host-specific serological response to Angiostrongylus vasorum infection in red foxes (Vulpes vulpes): implications for parasite epidemiology. Parasitol 144:1144–1153. https://doi.org/10.1017/S0031182017000427
Hajnalová M, Svobodová V, Schnyder M, Schaper R, Svoboda M (2018) Faecal detection of the lungworms Crenosoma vulpis and Angiostrongylus vasorum and serological detection of A. vasorum in dogs from the Czech Republic. Acta Vet Brno 86:393–398. https://doi.org/10.2754/avb201786040393
Hinaidy H (1971) Die Parasitenfauna des Rotfuchses, Vulpes vulpes (L.), in Österreich. Zbl Vet Med B 18:21–32. https://doi.org/10.1111/j.1439-0450.1971.tb00340.x
Koch J, Willesen JL (2009) Canine pulmonary angiostrongylosis: an update. Vet J 179:348–359. https://doi.org/10.1016/j.tvjl.2007.11.014
Lange MK, Penagos-Tabares F, Hirzmann J, Failing K, Schaper R, van Bourgonie Y, Backeljau T, Hermosilla C, Taubert A (2018) Prevalence of Angiostrongylus vasorum, Aelurostrongylus abstrusus and Crenosoma vulpis larvae in native slug populations in Germany. Vet Parasitol 254:120–130. https://doi.org/10.1016/j.vetpar.2018.03.011
Lassnig H, Prosl H, Hinterdorfer F (1998) Zur Parasitenfauna des Rotfuchses (Vulpes vulpes) in der Steiermark. Wien Tierärztl Mschr 85:116–122
Maier K, Löwenstein M, Duscher G, Leschnik M, Joachim A (2010) Angiostrongylus vasorum, der “französische Herzwurm”: auch ein Problem in Österreich? Wien Tierärztl Mschr 97:171–180
Miterpáková M, Schnyder M, Schaper R et al (2015) Serological survey for canine angiostrongylosis in Slovakia. Helminthologia 52:205–210. https://doi.org/10.1515/helmin-2015-0034
Penagos-Tabares F, Lange MK, Chaparro-Gutiérrez JJ, Taubert A, Hermosilla C (2018) Angiostrongylus vasorum and Aelurostrongylus abstrusus: neglected and underestimated parasites in South America. Parasit Vectors 11:208. https://doi.org/10.1186/s13071-018-2765-0
Penagos-Tabares F, Lange MK, Vélez J et al (2019) The invasive giant African snail Lissachatina fulica as natural intermediate host of Aelurostrongylus abstrusus, Angiostrongylus vasorum, Troglostrongylus brevior, and Crenosoma vulpis in Colombia. PLoS Negl Trop Dis. https://doi.org/10.1371/journal.pntd.0007277
Reifinger M, Greszl J (1994) Pulmonale Angiostrongylose mit systemischer Ausbreitung und zentralnervaler Manifestation bei einem Hund. J Veterinary Med Ser B 41:391–398. https://doi.org/10.1111/j.1439-0450.1994.tb00242.x
Taubert A, Pantchev N, Vrhovec MG, Bauer C, Hermosilla C (2009) Lungworm infections (Angiostrongylus vasorum, Crenosoma vulpis, Aelurostrongylus abstrusus) in dogs and cats in Germany and Denmark in 2003–2007. Vet Parasitol 159:175–180. https://doi.org/10.1016/j.vetpar.2008.10.005
Tolnai Z, Szell Z, Sreter T (2015) Environmental determinants of the spatial distribution of Angiostrongylus vasorum, Crenosoma vulpis and Eucoleus aerophilus in Hungary. Vet Parasitol 207:355–358. https://doi.org/10.1016/j.vetpar.2014.12.008
Traversa D, Di Cesare A, Conboy G (2010) Canine and feline cardiopulmonary parasitic nematodes in Europe: emerging and underestimated. Parasit Vectors 3:62. https://doi.org/10.1186/1756-3305-3-62
Walter T, Zink R, Laaha G, Zaller JG, Heigl F (2018) Fox sightings in a city are related to certain land use classes and sociodemographics: results from a citizen science project. BMC Ecol 18(1):50. https://doi.org/10.1186/s12898-018-0207-7
Zając KS, Gaweł M, Filipiak A, Kramarz P (2017) Arion vulgaris Moquin-Tandon, 1855 - the aetiology of an invasive species. Folia Malacol 25:81–93. https://doi.org/10.12657/folmal.025.008
Acknowledgements
We are particularly grateful to Mag. Alexandra Dockal-Penagos and Elfriede Dockal for their help during the slugs’ collection and Christine Henrich (Institute of Parasitology, Justus-Liebig-University Giessen, Germany) for her excellent technical assistance and support in molecular analyses of samples.
Funding
This research was funded by the Institute of Parasitology Justus-Liebig-University Giessen, Germany.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Section Editor: Domenico Otranto
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Supplementary Fig. 1
Alignment of ITS2-sequences of Aelurostrongylus larvae from Vienna snails and current GenBank entries (PDF 141 kb)
Rights and permissions
About this article
Cite this article
Penagos-Tabares, F., Groß, K.M., Hirzmann, J. et al. Occurrence of canine and feline lungworms in Arion vulgaris in a park of Vienna: First report of autochthonous Angiostrongylus vasorum, Aelurostrongylus abstrusus and Troglostrongylus brevior in Austria. Parasitol Res 119, 327–331 (2020). https://doi.org/10.1007/s00436-019-06527-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-019-06527-z