Subcutaneous ticks: a first report in a golden jackal, and their absence in non-canid carnivores

(2021) 14:5 Mechouk et al. Parasites Vectors https://doi.org/10.1186/s13071-020-04510-7 Parasites & Vectors Open Access SHORT REPORT Subcutaneous ticks: a first report in a golden jackal, and their absence in non‑canid carnivores Noureddine Mechouk1,2, Georgiana Deak2, Angela Monica Ionică2,3, Dan Traian Ionescu4*, Gabriel Bogdan Chișamera5, Călin Mircea Gherman2 and Andrei Daniel Mihalca2 Abstract Background: Ticks are hematophagous arthropods which normally attach to the surface of the host’s skin. Their aberrant presence in the subcutaneous tissue of a few carnivores, predominantly foxes, has been reported. However, there have been no reports of this phenomenon in other carnivores such as mustelids or golden jackals. Our aim was to investigate the host spectrum for this aberrant localization of ticks. Methods: Between 2015 and 2020, a total of 198 carcasses of 12 species of carnivore were examined by parasitological necropsy. When a subcutaneous tick was found, the nodule was removed, carefully dissected, and stored in ethanol. The morphological identification of the subcutaneous tick was carried out to species level. Results: A single subcutaneous tick was found in one carcass, that of a golden jackal (Canis aureus). The tick was identified as a female Ixodes ricinus. All the other carcasses were negative for the presence of subcutaneous ticks. Conclusion: To our knowledge, this is the first report of a subcutaneous tick in a golden jackal. This finding broadens the host spectrum of subcutaneous ticks, and reinforces the idea that, among carnivores, this phenomenon only occurs in canids. Keywords: Golden jackals, Subcutaneous, Ticks, Romania Background Ticks represent a large group of blood-sucking arthropods and are parasitic in a wide range of mammals, birds, reptiles, and occasionally amphibians. Ticks are also important vectors for various pathogens [1]. In ticks, a blood meal is required for molting, egg laying, and, in some species, preparation for mating [2]. Ticks typically attach to the external surface of the skin. However, there are reports of ticks being found in subcutaneous tissue (Table 1). Most of the reports of *Correspondence: 4 Department of Game and Wildlife, Faculty of Silviculture and Forestry Engineering, Transilvania University, Şirul Beethoven 1, 500123 Braşov, Romania Full list of author information is available at the end of the article subcutaneous ticks are from red foxes, with occasional findings in other carnivore hosts (a raccoon dog, and a domestic dog) (Table 1). So far, several hypotheses have been suggested to explain the presence of ticks in subcutaneous tissue, but none of them has been confirmed by experimental studies. It is unknown if the number of reports and the relatively common occurrence of subcutaneous ticks in red foxes is related to host preference or to the number of studies performed on this wild carnivore species. Hence, elucidating the full host spectrum of subcutaneous ticks is important to fill in the knowledge gaps for this phenomenon. It is also unclear why most of the reports on subcutaneous ticks are from eastern and central Europe, and if this geographical bias is related to the fact that foxes are the most widespread and studied wild canids in this area. During the last 20 © The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativeco mmons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Mechouk et al. Parasites Vectors (2021) 14:5 Page 2 of 4 years, the population of another canid, the golden jackal (Canis aureus) has increased significantly [3]. Golden jackals have an important role as reservoir hosts for parasites such as Leishmania infantum, Alaria alata, Dipylidium caninum, Mesocestoides lineatus, Trichinella spp., and Dirofilaria spp., and are also hosts for ticks [4]. Moreover, it is not clear if other wild carnivores such as mustelids can harbor subcutaneous ticks, as the lack of published reports could be a result of the lack of investigations. The aim of the present study was to investigate the occurrence of subcutaneous ticks in various species of wild carnivores in a geographical area where this aberrant localization is known to be prevalent in red foxes, in order to elucidate the role of the host species. Materials and methods Between 2015 and 2020, we necropsied 198 carcasses of 12 species of wild carnivores (57 golden jackals, six gray wolves, 19 wild cats, two Eurasian lynxes, 76 Eurasian badgers, 20 beech martens, eight European polecats, four European pine martens, three Eurasian otters, one stoat, one European mink, one least weasel) (Additional file 1) and examined them for parasites. The carcasses originated from roadkills or legally hunted animals. The carcasses were stored at −20 °C until processing. The age of the animals was estimated based on the state of tooth wear [5] and sexual maturity [6]. The carcasses were checked for the presence of ectoparasites, then necropsied using a standard method, starting with the removal of the skin. When subcutaneous ticks were found, the nodules were removed, carefully dissected, and stored in ethanol. The identification of the subcutaneous ticks was carried out to species level under an Olympus binocular magnifier and was based on taxonomic criteria according to dichotomous keys [1]. Results A single subcutaneous tick was found in one sample, a golden jackal, collected from Comana Natural Park, Romania (Fig. 1). The nodule was found under the skin of the left inguinal area. The tick was in an advanced stage of decomposition. However, despite the level of tick degradation, the gnathosoma and a large part of the idiosoma were well preserved, and the tick was identified as a female Ixodes ricinus. No subcutaneous ticks were found in the other examined carcasses. Discussion The mechanism causing the subcutaneous localization of ticks is still unknown, although several factors such as the species or the sex of the tick have been incriminated as favoring factors. A more common presence under the (...truncated)