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Endoparasites of European Wildcats (Felis Silvestris) in Greece

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Endoparasites of European Wildcats (Felis Silvestris) in Greece pathogens Article Endoparasites of European Wildcats (Felis silvestris) in Greece Anastasia Diakou 1,* , Despina Migli 2, Dimitris Dimzas 1, Simone Morelli 3 , Angela Di Cesare 3, Dionisios Youlatos 2 , Petros Lymberakis 4 and Donato Traversa 3 1 School of Veterinary Medicine, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece; [email protected] 2 School of Biology, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece; [email protected] (D.M.); [email protected] (D.Y.) 3 Faculty of Veterinary Medicine, University Teaching Veterinary Hospital, University of Teramo, 64100 Teramo, Italy; [email protected] (S.M.); [email protected] (A.D.C.); [email protected] (D.T.) 4 Natural History Museum of Crete, School of Sciences and Engineering, University of Crete, Knossou Avenue, 71409 Irakleio, Greece; [email protected] * Correspondence: [email protected] Abstract: The European wildcat (Felis silvestris) is the only wild felid living in Greece. Wildcat popu- lations are declining due to anthropogenic and phenological unfavourable conditions, and parasites may have an additional negative impact. In the present study, the occurrence of endoparasites in wildcats in Greece and the potential threats posed to wildcats, domestic animals, and humans in the study areas has been investigated. In a six-year period, 23 road-killed wildcats and 62 wildcat faecal samples were collected from different areas of the country. Necropsy for the detection of endopara- sites and standard parasitological examinations of faecal samples were performed. Parasites were morphologically identified and, in selected cases, molecularly analysed. All necropsied wildcats (100%) were infected by three to 10 different parasite taxa, with the most prevalent being Taenia Citation: Diakou, A.; Migli, D.; taeniaeformis (73.9%), Toxocara cati (60.9%), Angiostrongylus chabaudi (56.5%), Ancylostoma tubaeforme Dimzas, D.; Morelli, S.; Di Cesare, A.; (39.1%), Cylicospirura spp. (34.8%), Troglostrongylus brevior (34.8%), and Capillaria aerophila (33.8%). Of Youlatos, D.; Lymberakis, P.; Traversa, the 62 faecal samples examined, 53 (85.5%) were positive for one or more parasite elements (larvae, D. Endoparasites of European eggs, or oocysts). The most frequent were T. cati (45.2%), A. chabaudi (29%), C. aerophila (24.2%), and Wildcats (Felis silvestris) in Greece. Ancylostomatidae (17.7%). This is the first survey on endoparasites affecting wildcats in Greece. Pathogens 2021, 10, 594. https:// Some of the parasites here found are frequent in domestic and wild felids, while others, i.e., Oslerus doi.org/10.3390/pathogens10050594 rostratus and Cylicospirura petrowi, were described for the first time in the European wildcat. Most of them have a significant pathogenic potential, causing severe to hazardous diseases to infected felids Academic Editor: Lawrence S. Young and some, under specific circumstances, can also threaten human health. Received: 22 April 2021 Keywords: European wildcat; Felis silvestris; Greece; parasites Accepted: 12 May 2021 Published: 13 May 2021 Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in 1. Introduction published maps and institutional affil- The European wildcat, Felis silvestris (Carnivora, Felidae) is a small felid living in iations. areas of Europe and Asia (Figure1)[ 1,2]. Although it is listed as “Least Concern” by the International Union for Conservation of Nature and Natural Resources (IUCN), habitat loss and fragmentation as well as extensive hybridisation with domestic cats (Felis catus) have placed the species in an alerting conservation status [3]. These are important threats Copyright: © 2021 by the authors. causing a decreasing population trend, which has already resulted in veiled extinction in Licensee MDPI, Basel, Switzerland. some areas. In fact, an extended recent survey in different areas of Europe has revealed This article is an open access article varying hybridisation levels in the examined animals and has shown possible extinction of distributed under the terms and the Scottish population [2,4]. The European wildcat is the only wild felid with confirmed conditions of the Creative Commons reproducing populations in Greece and low levels of hybridisation, and it lives in several Attribution (CC BY) license (https:// habitats including agricultural areas and wetlands [4,5]. creativecommons.org/licenses/by/ 4.0/). Pathogens 2021, 10, 594. https://doi.org/10.3390/pathogens10050594 https://www.mdpi.com/journal/pathogens Pathogens 2021, 10, 594 2 of 23 Pathogens 2021, 10, x FOR PEER REVIEW 2 of 23 FigureFigure 1. 1.European European wildcat wildcat (Felis (Felis silvestris silvestris) distribution.) distribution. Coloured Coloured areas: areas: red red = present,= present, orange orange = pos-= possibly present, yellow = possibly extinct. The map was kindly provided by Peter Gerngross, MSc sibly present, yellow = possibly extinct. The map was kindly provided by Peter Gerngross, MSc [2]. [2]. (Reprinted with permission from ref. [2]. Copyright 2021 Gerngross, P. et al.). (Reprinted with permission from ref. [2]. Copyright 2021 Gerngross, P. et al.). OtherOther factorsfactors threateningthreatening thisthis felid felid species species are are human-caused human-caused mortality mortality (road (road kills kills andand poisoning) poisoning) andand competition competition withwith feral feral domestic domestic cats cats for for prey prey and and territory territory [ 2[2].]. The The interactioninteraction with with domestic domestic cats cats in in sympatric sympatric habitats habitats maymay also also result result in in disease disease transmis- transmis- sionsion andand both-ways-spill-overboth-ways-spill-over of pathogens, pathogens, such such as as parasites parasites [6,7]. [6,7 ].Parasitism Parasitism in inwild wild an- animalsimals is iscommon, common, and and its itsimpact impact is studied is studied under under three three perspectives: perspectives: (i) the (i) effect the effect of infec- of infections/infestationstions/infestations on the on wild the wild host, host, (ii) (ii)the thepossibility possibility of oftransmission transmission and and the the impact impact to todomestic domestic animals, animals, and and (iii) (iii) the the likelihood likelihood of implications onon humanhuman healthhealth [8[8].]. EvenEven thoughthough parasites parasites do do not not often often cause cause life-threatening life-threatening infections/infestations infections/infestations [ 8[8,9],,9], they they have have thethe potential potential to to undermine undermine the the wellbeing, wellbeing, health heal status,th status, and and overall overall fitness fitness of wild of wild animals, ani- includingmals, including the ability the ability to prey, to mate, prey, and mate, escape and predators.escape predators. Thus, under Thus, certain under conditions,certain con- parasitesditions, parasites are a significant are a significant threat for threat vulnerable for vulnerable populations populations [10]. [10]. KnowledgeKnowledge onon parasitesparasites affecting European European w wildcatsildcats is is scant, scant, due due to tothe the elusive elusive na- natureture of of these these animals animals and and minimum minimum interactions interactions with humans, whichwhich renderrender challenging challenging anyany sample sample collections. collections. However,However, inin thethe recent recent years, years, the the scientific scientific interest interest on on parasites parasites affectingaffecting wild wild felids felids has has increased increased significantly, significantly, as novelas novel insights insights have have shed shed light light on possible on pos- bridgingsible bridging infections infections with with cardiopulmonary cardiopulmonary nematodes nematodes between between wildcats wildcats and and domestic domes- catstic cats [7,11 [7,11–14].–14]. Recent Recent data data have have suggested suggested that that domestic domestic cats cats in in Greece Greece may may be be infected infected byby parasites parasites and and vector-borne vector-borne pathogens, pathogens, which which could could be be shared shared by by wildcats wildcats and and in in some some casescases havehave thethe potentialpotential to also infect infect dogs dogs and and humans humans [15–21]. [15–21]. Additionally, Additionally, single single re- reportsports of of multiparasitism multiparasitism in in two two wildcats in GreeceGreece andand BosniaBosnia andand Herzegovina Herzegovina have have clearlyclearly provedproved thatthat heavy parasitic parasitic infections infections may may represent represent a factual a factual threat threat for forthese these ani- animalsmals [22,23]. [22,23 Therefore,]. Therefore, the the aim aim of the of the presen presentt survey survey was was to investigate to investigate in a in focused a focused epi- epizootiological,zootiological, large-scale large-scale study, study, the the occurrence occurrence of of endoparasi endoparasitestes in wildcatswildcats inin GreeceGreece by by faecalfaecal and and post-mortem post-mortem examinations, examinations, and and to assessto assess the the potential potential threats threats posed posed to wildcats, to wild- domesticcats, domestic animals, animals, and humans and humans in the in study the study areas. areas. 2.2. Materials Materials and and Methods Methods 2.1. Study Areas, Animals, and Samples 2.1. Study Areas, Animals, and Samples From 2015 to 2021, road-killed wildcats and faecal samples were collected from From
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