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Taeniid Cestodes in a Wolf Pack Living in a Highly Anthropic Hilly Agro-Ecosystem

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Taeniid Cestodes in a Wolf Pack Living in a Highly Anthropic Hilly Agro-Ecosystem Parasite 28, 10 (2021) Ó F. Macchioni et al., published by EDP Sciences, 2021 https://doi.org/10.1051/parasite/2021008 Available online at: www.parasite-journal.org RESEARCH ARTICLE OPEN ACCESS Taeniid cestodes in a wolf pack living in a highly anthropic hilly agro-ecosystem Fabio Macchioni1,a, Francesca Coppola1,a, Federica Furzi2, Simona Gabrielli2, Samuele Baldanti1, Chiara Benedetta Boni1, and Antonio Felicioli1,* 1 Department of Veterinary Sciences, University of Pisa, Viale delle Piagge 2, 56124 Pisa, Italy 2 Department of Public Health and Infectious Diseases, Sapienza University of Rome, Piazzale Aldo Moro 5, 00185 Rome, Italy Received 24 September 2020, Accepted 24 January 2021, Published online 5 February 2021 Abstract – The Italian wolf population in human-modified landscapes has increased greatly in the last few decades. Anthropisation increases the risk of transmission of many zoonotic infections and in this context, control of taeniid cestode species needs to be addressed from a One Health perspective. Predator-prey interactions are at the root of taeniid cestode transmission, and the wolf plays a key role in the maintenance and transmission of taeniids. To date, all available data on the taeniids of wolves in Italy refer to populations living in a wild habitat. Between 2018 and 2019, we investigated taeniids in a wolf pack living in a highly anthropic hilly agro-ecosystem. Thirty-eight faecal samples were collected and analysed, 4 of which were also genetically characterised for individual wolves and belonged to three different animals. Samples collected were analysed microscopically and by molecular analysis in order to identify the taeniid species. Taeniid eggs were detected in 34.2% (13/38) of samples. Within samples positive to taeniid eggs only Echinococcus granulosus s.s. and Taenia hydatigena were identified in 26.3% and 10.5% of the samples, respectively. On microscopic examination, Capillaria spp., Ancylostomatidae and Toxocara canis eggs, Crenosoma vulpis larvae, and coccidian oocysts were also found. The combination of low biodiversity of taeniid species with a high occurrence of E. granulosus s.s. recorded in this study could be the consequence of a deeper link occurring between wolves and livestock in human-modified landscapes than in wild settings. Key words: Anthropic areas, Canis lupus, Echinococcus granulosus s.s., Taenia hydatigena, Helminths, Parasites. Re´sume´ – Cestodes Taeniidae dans une meute de loups vivant dans un agroécosystème vallonné hautement anthropique. La population de loups italiens dans les paysages modifiés par l’homme a considérablement augmenté au cours des dernières décennies. L’anthropisation augmente le risque de transmission de nombreuses infections zoonotiques et, dans ce contexte, le contrôle des espèces de cestodes Taeniidae doit être abordé dans une perspective One Health. Les interactions prédateurs-proies sont à la base de la transmission des Cestodes Taeniidae, et le loup joue un rôle clé dans le maintien et la transmission des Taeniidae. À ce jour, toutes les données disponibles sur les Taeniidae du loup en Italie se réfèrent aux populations vivant dans un habitat sauvage. Entre 2018 et 2019, les Taeniidae d’une meute de loups vivant dans un agro-écosystème vallonné hautement anthropique ont été étudiés. Trente-huit échantillons fécaux ont été collectés et analysés, dont quatre ont également été génétiquement caractérisés pour des loups individuels et appartenaient à trois animaux différents. Les échantillons prélevés ont été analysés au microscope et par analyse moléculaire afind’identifier les espèces de Taeniidae. Des œufs de Taeniidae ont été détectés dans 34,2 % (13/38) des échantillons. Dans les échantillons positifs aux œufs de Taeniidae, seul Echinococcus granulosus s.s. et Taenia hydatigena ont été identifiés dans 26,3 % et 10,5 % des échantillons, respectivement. Lors de l’examen microscopique, des œufs de Capillaria spp., d’Ancylostomatidae et de Toxocara canis, des larves de Crenosoma vulpis et des oocystes de coccidie ont également été trouvés. La combinaison d’une faible biodiversité d’espèces de Taeniidae avec une forte occurrence d’E. granulosus s.s. rapportées dans cette étude pourrait être la conséquence d’un lien plus profond entre le loup et le bétail dans les paysages humains que dans les paysages sauvages. *Corresponding author: [email protected] aThese authors contributed equally to this work. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. 2 F. Macchioni et al.: Parasite 2021, 28,10 Introduction T. krabbei, T. ovis, E. multilocularis and E. granulosus s.s. were also found in low frequency [22, 23, 37, 49]. The family Taeniidae includes four genera: Taenia Within the E. granulosus s.l. species cluster, E. granulosus Linnaeus, 1758, Echinococcus Rudolphi, 1801, Hydatigera s.s. and E. canadensis are mainly detected in wolves [23, 49, Lamarck, 1816), and Versteria Nakao, Lavikainen, Iwaki, 57]. Echinococcus granulosus s.s., the major cause of cystic Haukisalmi, Konyaev, Oku, Okamoto & Ito, 2013, which echinococcosis (CE) in humans in the world [1], is highly parasitise both mammals and humans [33, 47, 59]. Within the endemic in the Mediterranean basin, particularly in rural genera Taenia and Echinococcus, Taenia solium, Taenia livestock-raising areas [10]. In these areas, the prevalence of saginata, Echinococcus granulosus s.l.andEchinococcus E. granulosus s.l. in wolves is closely linked to the semi- multilocularis are important pathogens causing food-borne domestic cycle as a consequence of the high prevalence of zoonotic infections worldwide [15]. Tapeworm transmission cystic echinococcosis in sheep [24, 49]. is based on indirect domestic, semi-domestic and wildlife cycles Since no data are available on the Taeniidae population in involving various mammalian hosts including: (i) wild or wolves living in newly colonised, highly anthropic areas, the domestic herbivores (prey), or (ii) wild or domestic canids or aim of this study was to investigate the Taeniidae in a wolf pack felids (predators) [33]. Occasionally, certain other zoonotic living in a highly anthropic hilly agroecosystem using non- tapeworm species can also infect humans [33]. invasive sampling. We predicted that in such areas, Taeniidae Predator–prey interactions are at the root of taeniid trans- species from domestic intermediate hosts would be the most mission, in which predators are the definitive hosts, while the frequently recorded species associated with low taeniid biodi- prey is the intermediate host. This is referred to as a multi-host versity as a consequence of a deeper link occurring between trophically-transmitted parasite system [3]. wolves and livestock in human-modified landscapes than in Among definitive hosts, the wolf (Canis lupus)playsakey wild environments. role in the maintenance and transmission of several Taeniidae and could serve as a model species to better understand prey–predator and host–parasite dynamics [20]. Due to its top Materials and methods position in the wild trophic chain, the wolf hosts a wide gas- Study area trointestinal parasite community, which changes in relation to its diet [20]. The study was carried out in a sub-urban, hilly area in As an opportunistic predator, the wolf selects its preys Crespina-Lorenzana and Lari-Casciana Terme (43.551370°– according to their local abundance, accessibility and vulnerabil- 10.551708°) in the Province of Pisa (central Italy). The study ity [39–41]. In Italy, the wolf’s diet is mainly based on wild area of 900 ha is a highly anthropic, sub-urban, hilly, ungulates such as wild boar (Sus scrofa), roe deer (Capreolus fragmented, woody agro-ecosystem where a wide variety of capreolus), red deer (Cervus elaphus) and fallow deer wildlife mammals live, such as crested porcupines (Hystrix cris- (Dama dama), but it also preys upon livestock, especially goats tata), wild boar (Sus scrofa), roe deer (Capreolus capreolus), (Capra hircus), sheep (Ovis aries) and calves (Bos taurus) pine martens (Martes martes), stone martens (Martes foina), [16, 32, 39, 42]. European polecats (Mustela putorius), badgers (Meles meles), The Italian wolf population (C. lupus italicus,Altobello hares (Lepus europaeus), eastern cottontails (Sylvilagus 1921), was in strong decline until the 1970s [60]; however, floridanus), wild rabbits (Oryctolagus cuniculus), red foxes in the last few decades it has undergone natural re-expansion (Vulpes vulpes), and a large variety of small mammals. In the throughout the Alps and Apennines and in human-modified study area, small, woody areas are interspersed with human environments [14, 21]. settlements, which lead to intensive interactions between the The wolf’s legal protection in Italy, which was established wildlife and productive and recreational activities of humans in 1976, together with changes in the ecology of mountain areas (i.e. sheep farming, forest cutting, trekking, cycling, horse (e.g. decrease in human density and an increase in wild ungu- riding, bird watching, and hunting). The study area includes lates) as well as the natural reforestation of these areas, have 18 villages, with an average human density of 134.08 people/ promoted the wolf’s re-colonisation of its historical distribution km2. Extensive or semi-extensive sheep and cattle farming range
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