Metastrongyloid nematodes typically reside as adults in the cardiopulmonary systems of their mammalian definitive hosts, potentially causing severe diseases. Of particular concern are Angiostrongylus cantonensis and A. costaricensis, which can cause eosinophilic meningitis and abdominal angiostrongyliasis, respectively, in their accidental human hosts. Several metastrongyloid species of medical and veterinary importance have been documented in the Canary Islands. However, the gastropod species acting as intermediate hosts for some of these nematodes in the archipelago remained unknown. This study aimed to investigate the occurrence of metastrongyloid nematodes in terrestrial and aquatic gastropods, including both endemic and non-native species, on Tenerife. Foot samples from terrestrial and aquatic gastropods were analyzed using a multiplex PCR targeting the Internal Transcribed Spacer 1 (ITS1), allowing the specific detection of A. cantonensis, A. vasorum, Aelurostrongylus abstrusus, Crenosoma striatum, Troglostrongylus brevior, and Crenosoma vulpis. Five metastrongyloid species, namely C. striatum, A. cantonensis, Ae. abstrusus, A. vasorum, and an unidentified metastrongyloid, were identified within both non-native and endemic terrestrial gastropods. In the aquatic snail Physella acuta, only A. cantonensis and C. striatum were detected. This study confirms the introduction of various metastrongyloids associated with non-native mammalian fauna and provides new data on the occurrence of these nematodes in non-native and endemic gastropod species, including their presence in aquatic environments on the Canary Islands.

Departamento de Obstetricia y Ginecología Pediatría Medicina Preventiva y Salud Pública Toxicología Medicina Legal y Forense y Parasitología Facultad de Farmacia Universidad de La Laguna San Cristóbal de La Laguna Spain

Department of Botany and Zoology Faculty of Science Masaryk University Brno Czech Republic

Department of Chemistry and Biochemistry Mendel University Brno Czech Republic

Department of Veterinary Sciences Faculty of Agrobiology Food and Natural Resources CINeZ Czech University of Life Sciences Prague Prague Czech Republic

Faculty of Medicine in Pilsen Biomedical Center Charles University Plzeň Czech Republic

Institute of Parasitology Biology Center of Czech Academy of Sciences České Budějovice Czech Republic

Instituto Universitario de Enfermedades Tropicales y Salud Pública de Canarias Universidad de La Laguna San Cristóbal de La Laguna Spain

Zobrazit více v PubMed

Alicata JE (1965) Biology and distribution of the rat lungworm, Angiostrongylus cantonensis, and its relationship to eosinophilic meningoencephalitis and other neurological disorders of man and animals. Adv Parasitol 223-48. https://doi.org/10.1016/S0065-308X(08)60366-8

Alto W (2001) Human infections with Angiostrongylus cantonensis. Pac Health Dialog 8(1):176–182 PubMed

Anderson RC (2000) Nematode parasites of vertebrates: their development and transmission, 2nd edn. Cabi Publish, Wallingford DOI

Anettová L, Izquierdo-Rodriguez E, Foronda P, Baláž V, Novotný L, Modrý D (2022) Endemic lizard Gallotia galloti is a paratenic host of invasive Angiostrongylus cantonensis in Tenerife. Spain Parasitol 149(7):1–23

Arechavaleta M, Rodríguez S, Zurita N, García A (2010) Lista de Especies Silvestres de Canarias. Hongos, Plantas y Animales Terrestres. Gobierno de Canarias, Santa Cruz de Tenerife, Spanish

Barone Tosco R (2018) Vertebrados. In: Revisión de la lista de las especies de vertebrados terrestres de Canarias, así como la georreferenciación de las especies de aves migrantes del archipiélago, para su registro en el Banco de Datos de Biodiversidad de Canarias, cofinanciado por el programa operativo FEDER CANARIAS (2014–2020). Gobierno de Canarias, Consejería de Medio Ambiente y Ordenación Territorial

Baruš V, Blažek K (1971) The life cycle and the pathogenicity of the nematode Crenosoma striatum (Zeder, 1800). Parasitol 18(3):2015–2026

Brianti E, Gaglio G, Giannetto S, Annoscia G, Latrofa MS, Dantas-Torres F, Traversa D, Otranto D (2012) Troglostrongylus brevior and Troglostrongylus subcrenatus (Strongylida: Crenosomatidae) as agents of broncho-pulmonary infestation in domestic cats. Parasit Vectors 5(1):1–12 PubMed DOI PMC

Carracedo JC, Pérez-Torrado FJ (2013) Geological and geodynamic context of the teide volcanic complex. In: Carracedo JC, Troll VR (eds) Teide Volcano, active volcanoes of the world. Springer-Verlag, Berlin Heidelberg

Courchamp F, Chapuis JL, Pascal M (2003) Mammal invaders on islands: impact, control and control impact. Biol Rev 78:347–383 PubMed DOI

Cowie RH (2019) Annotated catalogue of species of Angiostrongylus and the related genera Gallegostrongylus, Rodentocaulus and Stefanskostrongylus (Nematoda: Metastrongyloidea, Angiostrongylidae). J Helminthol 93(4):389–423 PubMed DOI

Deak G, Ionică AM, Gherman CM, Mihalca AD (2023) Diversity of Crenosoma species in mustelids with the first molecular characterization of C. melesi and C. petrowi. Front Vet Sci 10:1094554 PubMed DOI PMC

Foronda P, López-González M, Miquel J, Torres J, Segovia M, Abreu-Acosta N, Casanova JC, Valladares B, Mas-Coma S, Bargues MD, Feliu C (2010) Finding of Parastrongylus cantonensis (Chen, 1935) in Rattus rattus in Tenerife, Canary Islands (Spain). Acta Trop 114(2):123–127 PubMed DOI

Francis EK, Šlapeta J (2022) A new diagnostic approach to fast-track and increase the accessibility of gastrointestinal nematode identification from faeces: FECPAKG2 egg nemabiome metabarcoding. Int J Parasitol 52(6):331–342 PubMed DOI

García Livia K, Reyes R, Amaro-Ramos V, Baz-González E, Martin-Carrillo N, Rodríguez-Ponce E, Foronda P (2023) Metastrongyloid infection with Aelurostrongylus abstrusus, Troglostrongylus brevior, Oslerus rostratus and Angiostrongylus chabaudi in feral cats from the Canary Islands (Spain). Animals 13(13):2168 PubMed DOI PMC

Halvarsson P, Baltrušis P, Kjellander P, Höglund J (2022) Parasitic strongyle nemabiome communities in wild ruminants in Sweden. Parasit Vectors 15(1):1–15 DOI

Hamilton JM (1963) Aelurostrongylus abstrusus infestation of the cat. Vet Rec 76(16):417–422

Hobmaier M, Hobmaier A (1935) Intermediate hosts of Aelurostrongylus abstrusus of the cat. Exp Biol Med 32:1641 DOI

Izquierdo-Rodriguez E, Anettová L, Hrazdilová K, Foronda P, Modrý D (2023) Range of metastrongylids (superfamily Metastrongyloidea) of public health and veterinary concern present in livers of the endemic lizard Gallotia galloti of Tenerife, Canary Islands. Spain Parasites Vectors 16:81 PubMed DOI

Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28(12):1647–1649 PubMed DOI PMC

Kennerley R (2019) Crocidura canariensis. The IUCN Red List of Threatened Species 2019. e.T5560A3031266.  https://doi.org/10.2305/IUCN.UK.2019-1.RLTS.T5560A3031266.en

Kretschmar F (2016) Die Parasiten des Europäischen Iltisses Mustela putorius Linnaeus, 1758 in Deutschland. Faculty of Veterinary Medicine. Ludwig-Maxilians-Universität München, German

Kim JR, Hayes KA, Yeung NW, Cowie RH (2014) Diverse gastropod hosts of Angiostrongylus cantonensis, the rat lungworm, globally and with a focus on the Hawaiian Islands. PLoS ONE 9(5):e94969 PubMed DOI PMC

Lange MK, Penaggos-Tabares F, Hirzmann J, Failing K, Schaper R, Van Bourgonie YR, 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 PubMed DOI

Maksimov P, Hermosilla C, Taubert A, Staubach C, Sauter-Louis C, Conraths FJ, Vrhovec MG, Pantchev N (2017) GIS-supported epidemiological analysis on canine Angiostrongylus vasorum and Crenosoma vulpis infections in Germany. Parasites Vectors 10(1):1–14 DOI

Martin-Alonso A, Abreu-Yanes E, Feliu C, Mas-Coma S, Bargues MD, Valladares B, Foronda P (2015) Intermediate hosts of Angiostrongylus cantonensis in Tenerife, Spain. Plos One 10(3):e0120686 PubMed DOI PMC

Martin-Carrillo N, Baz-González E, García-Livia K, Amaro-Ramos V, Abreu-Acosta N, Miquel J, Abreu-Yanes E, Pino-Vera R, Feliu C, Foronda P (2023) Data on new intermediate and accidental hosts naturally infected with Angiostrongylus cantonensis in La Gomera and Gran Canaria (Canary Islands, Spain). Animals 13(12):1969 PubMed DOI PMC

Martin-Carrillo N, Feliu C, Abreu-Acosta N, Izquierdo-Rodriguez E, Dorta-Guerra R, Miquel J, Abreu-Yanes E, Martin-Alonso A, García-Livia K, Quispe-Ricalde MA, Serra-Cobo J, Valladares B, Foronda P (2021) A peculiar distribution of the emerging nematode Angiostrongylus cantonensis in the Canary Islands (Spain): recent introduction or isolation effect? Animals 11(5):1267 PubMed DOI PMC

Medina FM, Nogales M (2009) A review on the impacts of feral cats (Felis silvestris catus) in the Canary Islands: implications for the conservation of its endangered fauna. Biodivers Conserv 18:829–846 DOI

Medina FM, Martin A (2010) A new invasive species in the Canary Islands: a naturalized population of ferrets Mustela furo in La Palma Biosphere Reserve. Oryx 44(1):41–44. https://doi.org/10.1017/S0030605309990743

MolluscaBase eds (2023) MolluscaBase. https://www.molluscabase.org . Accessed 2023–09–05. https://doi.org/10.14284/448

Morgan ER, Shaw SE, Brennan SF, De Waal TD, Jones BR, Mulcahy G (2005) Angiostrongylus vasorum: a real heartbreaker. Trends Parasitol 21(2):49–51 PubMed DOI

Nogales M, Rodríguez-Luengo JL, Marrero P (2006) Ecological effects and distribution of invasive non-native mammals on the Canary Islands. Mammal Rev 36(1):49–65 DOI

Pafčo B, Čížková D, Kreisinger J, Hasegawa H, Vallo P, Shutt K, Todd A, Petrželková KJ, Modrý D (2018) Metabarcoding analysis of strongylid nematode diversity in two sympatric primate species. Sci Rep 8(1):5933 PubMed DOI PMC

Pino R, Izquierdo E, Rodríguez JL, Foronda P (2021) Los lagartos endémicos en la dieta de los hurones asilvestrados en Canarias: impacto en la conservación. Bol Asoc Herpetol Esp 32(1):159–160

Rodríguez-Ponce E, González JF, de Felipe MC, Hernández JN, Jaber JR (2016) Epidemiological survey of zoonotic helminths in feral cats in Gran Canaria Island (Macaronesian archipelago-Spain). Acta Parasitol 61(3):443–450 PubMed DOI

Romero-Alegría A, Belhassen-García M, Velasco-Tirado V, García-Mingo A, Alvela-Suárez L, Pardo-Lleidas JP, Cordero Sánchez M (2014) Angiostrongylus costaricensis: systematic review of case reports. Adv Infect Dis 4(1):36–41

Sánchez Vicente S (2013) Contribución al conocimiento de la parasitofauna (Helmintos y Artrópodos) de mamíferos no lagomorfos de Canarias. Departament de Microbiologia i Parasitologia Sanitàries, Universitat de Barcelona. Spanish, Barcelona

Segeritz L, Cardona A, Taubert A, Hermosilla C, Ruiz A (2021) Autochthonous Angiostrongylus cantonensis, Angiostrongylus vasorum and Aelurostrongylus abstrusus infections in native terrestrial gastropods from the Macaronesian Archipelago of Spain. Parasitol Res 120:2671–2680 PubMed DOI PMC

Van Dyke F (2008) Conservation biology: foundations, concepts, applications. Springer Science & Business Media DOI