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Introduction
Altered ecosystem dynamics and the increasing interaction between humans, domestic animals, and wildlife are an important source of zoonotic diseases (Bengis et al., 2004; Polley, 2005, Myers et al., 2013; Rizzoli et al., 2019; Magouras et al., 2020). These are defined as those infectious illnesses of animal origin that can affect humans. Worldwide, parasites serve as transmission vectors for 35 % of these afflictions (Vélez-Hernández et al., 2014), where the probability of acquisition is defined by ecological (Gibb et al., 2020) and biological factors of humans, the disease, the vector, and its host (Polley, 2005; Rizzoli et al., 2019; Sooksawasdi Na Ayudhya & Kuiken, 2021).
Among mammals, the order Carnivora harbors the largest number of zoonotic pathogens and parasites. Especially the taxonomic family of procyonids, which has been recognized for its role in the transmission of various pathogens of parasitic origin to humans (Han et al., 2021). There is information about the coati Nasua narica (Linnaeus, 1766) and the raccoon Procyon lotor (Linnaeus, 1758), whose wide distribution, proximity to human settlements, omnivorous diet, dispersal capacity over long distances, and the use of latrines, contribute to the health hazard. However, there are few reports of zoonoses by other procyonid species, such as the ringtail cat Bassariscus astutus (Lichtenstein, 1830), despite having a similar life history and behavior. There is little information on the ecology and biology of this species, as well as its role as a vector or reservoir of parasites. For this reason, this study aimed to compile and synthesize the available information on the species that parasitize the ringtail cat. This information will make it possible to identify areas of opportunity for future studies on the species, its parasites, and the interactions they have with other organisms, including humans.
Material and Methods
A systemic review of the metazoan species that parasitize B. astutus was carried out based on the PRISMA checklist (Preferred Reporting Items for Systematic Reviews and Meta-Analyses; Page et al., 2021). The registered parasites were divided into two categories: ectoparasites and endoparasites. For the former, the arthropod phylum was investigated, which includes most of the organisms that infect mammals (Balashov, 2006). While for endoparasites, various taxonomic groups were included, such as helminths (Acanthocephali, cestodes, trematodes, nematodes, etc.) and protists (Apicomplexa, Euglenozoa, etc.).
The data search was carried out in scientific journals, university newsletters, documents of scientific societies, technical reports, and books published between 1900 and 2021. Initially, it was carried out in the databases of Google Scholar, EBSCOhost, JSTOR, ScienceDirect, PubMed, and Scielo Scientific Library. In which, the following keywords were entered in independent searches: “Bassariscus astutus”, “ringtail cat”, “cacomixtle” “cacomiztle”, “mammals”, “carnivores”, “wildlife” and “parasites”, “host - parasites”, “ectoparasites”, “endoparasites”, “Ixodes”, “ticks”, “fleas”, “Helminths”, “infectious disease”, “T. cruzi”, “Toxoplasmosis” and “Mexico”, “Arizona, “New Mexico”, “Texas”, “California”, “Nevada”, “Utah, “Colorado”. The same keywords were translated and used in Spanish.
The information on the parasite species reported and cited within the studies was used to build a table, which included the following qualitative variables: year of publication, study area, phylum, type of parasite (endoparasites/ectoparasites), habitat (tract gastrointestinal, lungs, heart, blood, epidermis, etc.) and if it acts as the causative agent or vector of any disease of medical interest considered by the Pan American Health Organization (PAHO, 2003). Once the information was collected, a map and a line graph were used to evaluate the trend in the location and number of documents published every five years since 1900 and to identify the most studied parasite phyla in B. astutus. The relative frequency for the type of habitat was calculated and a Chi-square test was performed to analyze if there were significant differences between ectoparasites and endoparasites. Additionally, a species accumulation curve was built considering each publication as a sampling unit; The EstimateS program (version 9.1.0) was used to randomize the information and calculate the biodiversity estimators Chao1, Chao2, Jack1, Jack2, and Bootstrap, and R (R Core Team 2019) to build a curve for each estimator.
Results and Discussion
A total of 23 publications about the species that parasitize Bassaricus astutus were identified and included in the present review ( Appendix 1). Of the evaluated literature, four texts explicitly contained the name of B. astutus or its common name within the title; 14 alluded to ectoparasites, specifically ticks, the genus Ixodes, and/or their hosts; and five to T. cruzi and diseases in wild mammals. However, at least one species of parasite present in B. astutus was mentioned. The results presented a bias towards more recent studies, some works published at the beginning of the 20th century were not possible to find and include in the present review (i.e., Neumann (1911) cited by Cooley & Kohls (1945); Mac-Callum (1921), and Price (1928) cited by Pence & Willis (1978)). Thus, the information corresponded to a period of 76 years, with an average of 1.5 publications every 5 years, with an increase in number between 1970-1975 and 2000-2005 (Figure 1). Regarding their origin, they came mainly from the United States (n=17; 70 % in Texas, 15 % in Nevada, Arizona, and New Mexico, and 11 % without a specific location within the country), followed by Mexico (n=7; 28 % in Nuevo León, 28 % in Mexico City and the rest in Baja California Sur, Guanajuato and Guerrero) as can be seen in Figure 2.
Data was gathered on the occurrence of 55 parasite species belonging to the following phylum: Acanthocephala (1), Apicomplexa (1), Arthropoda (46), Euglenozoa (1), Nematoda (3) and Platyhelminthes (3); with a significant difference between the studies of ectoparasites and endoparasites (χ 2(22, N=23) = 59.08, p > 0.05), where 83 % of the species were arthropod ectoparasites present in the epidermis and fur of B. astutus, with few others distributed in other body areas (Figure 3). This bias could be since most of the reports came mainly from ectoparasite-host lists, where B. astutus was not usually the study subject (for example: Beck et al., 1963; Montiel-Parra et al., 2007 and Guzmán-Cornejo et al., 2007). Furthermore, the limited number of publications on endoparasites, which account for only 16 % of the species, may be attributed to the challenges associated with accessing samples. This difficulty arises due to the non-random distribution of B. astutus latrines, which are typically found in hard-to-reach locations with steep slopes or elevated positions (Barja & List, 2006). Additionally, the activity patterns and habitat preference of B. astutus can make it difficult to capture for biopsies (Ryser-Degiorgis, 2013). The reduced number of publications, added to the few places where they were made, leave aside species of parasites that could be associated with a particular ecoregion (Kresta et al., 2009), and do not show the temporal and spatial fluctuation that could exist among parasitic communities. Therefore, it is highly probable that there are more than 55 species of parasites in B. astutus (Appendix 1).
Of the reported parasites, the most cited taxonomic families were Ixodidae and Pulicidae. This could be partially explained because they have complex life cycles that require different hosts and that generally do not present specificity when infecting other species (Cañizales & Guerrero, 2017). The presence of the Ctenocephalides felis flea could be considered anomalous in B. astutus since this species usually resides in the domestic cat, although it has also been found in other mammals (Durden & Traub, 2002). In contrast, the louse Neotrichodectes thoracicus and the cestode Taenia pencei have only been reported on B. astutus so far (Osborn, 1902; Ewing, 1936; Emerson & Roger, 1985; Rausch, 2003; Kelley & Horner, 2008), which could indicate some level of specificity of both parasites.
In relation to the diversity of parasite species, it was determined that, both in the observed and estimated species, the asymptotic number was not reached (Figure 4). Hence, the parasite inventory of this work can be considered incomplete. The Jack1, Jack2 and Chao2 estimators overestimated species richness and presented greater bias. For example, Chao2 predicts that more than 70 species remain to be reported to reach the total asymptote of the curve. On the other hand, the Chao1 and Bootstrap estimators presented less bias and were more precise. Both estimators predict that around 20 species remain to be inventoried for the census to be complete. The behavior of the estimators coincides with that reported by Poulin (1998), Romero-Tejeda et al. (2008) and Bautista-Hernández et al. (2013); who, for parasitology studies, mention that the most recommended wealth estimator is Bootstrap.
Eight parasite species were identified in B. astutus, which cause or serve as a vector for 14 zoonoses considered by PAHO (2003). 14.28 % of them are caused by protists, 28.57 % by cestodes, and 57.14 % by ticks of the Ixodidae family. The reported seroprevalence for Toxoplasma gondii in B. astutus in suburban environments was 20 % (Suzán & Ceballos, 2005) and in South Texas for Chagas disease 100 % (Kramm et al., 2019). However, B. astutus is not considered to be a reservoir for either of these two protozoa since the reports are scarce and come from few samples. In relation to helminthiasis, the most noteworthy are coenurosis, taeniasis, and mesocestoidiasis, caused mainly by the genera Taenia and Mesocestoides. The prevalence of Mesocestoides of 20 % found by Pence & Willis (1978) could indicate that B. astutus serves as the definitive host for these organisms, since according to Chelladurai & Brewer (2021) the prevalence of Mesocestoides in intermediate hosts is 7.09 % and in definitive hosts 21.72 %. Regarding pathologies caused by arthropods, to date it has not been investigated whether B. astutus plays any role in the natural history of these pathogens. However, it is important to highlight that ticks of the genera Haemaphysalis, Dermacentor, Ixodes, and Amblyomma (all identified in B. astutus) are responsible for the storage and transmission of most zoonoses among arthropods (Sosa-Gutierrez et al., 2016; Rizzoli et al., 2019). Although the dynamics between B. astutus and zoonoses remain unknown, the species could be considered as an indicator of the parasites present in an ecosystem (Han et al., 2021). This is important as, among wildlife-transmitted zoonoses, the discovery rate of new parasites is low relative to bacteria and viruses (Polley, 2005).
Conclusions
Information was collected on 55 species that parasitize B. astutus from 23 scientific articles published for more than 76 years. The collected data showed a bias towards ectoparasites, which means that greater research effort towards endoparasites is required. We identified that the louse Neotrichodectes thoracicus and the cestode Taenia pencei may present some type of specificity towards B. astutus. The species accumulation curve showed that more than 20 taxa still need to be identified to complete the inventory of parasites of the species. Finally, more information is needed to identify temporal and spatial patterns between B. astutus and its parasites as well as to recognize whether B. astutus plays a role as a reservoir or vector of zoonotic diseases.
