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Role of Zoo-Housed Animals in the Ecology of Ticks and Tick-Borne Pathogens—A Review

Johana Hrnková
Irena Schneiderová
Marina Golovchenko
Libor Grubhoffer
Natalie Rudenko
4 and
Jiří Černý
Centre for Infectious Animal Diseases and Zoonoses, Faculty of Tropical AgriSciences, Czech University of Life Sciences Prague, Kamýcká 129, Prague 6, 165 00 Suchdol, Czech Republic
Department of Animal Science and Food Processing, Faculty of Tropical AgriSciences, Czech University of Life Sciences Prague, Kamýcká 129, Prague 6, 165 00 Suchdol, Czech Republic
Department of Zoology, Faculty of Science, Charles University, Viničná 7, 2 128 00 Prague, Czech Republic
Institute of Parasitology, Biology Centre, Czech Academy of Sciences, Branišovská 1160/31, 370 05 České Budějovice, Czech Republic
Faculty of Sciences, University of South Bohemia, Branišovská 1160/31, 370 05 České Budějovice, Czech Republic
Author to whom correspondence should be addressed.
Pathogens 2021, 10(2), 210;
Submission received: 14 January 2021 / Revised: 11 February 2021 / Accepted: 13 February 2021 / Published: 16 February 2021
(This article belongs to the Special Issue Ticks and Tick-Borne Diseases―Pathogens, Parasites and People)


Ticks are ubiquitous ectoparasites, feeding on representatives of all classes of terrestrial vertebrates and transmitting numerous pathogens of high human and veterinary medical importance. Exotic animals kept in zoological gardens, ranches, wildlife parks or farms may play an important role in the ecology of ticks and tick-borne pathogens (TBPs), as they may serve as hosts for local tick species. Moreover, they can develop diseases of varying severity after being infected by TBPs, and theoretically, can thus serve as reservoirs, thereby further propagating TBPs in local ecosystems. The definite role of these animals in the tick–host-pathogen network remains poorly investigated. This review provides a summary of the information currently available regarding ticks and TBPs in connection to captive local and exotic wildlife, with an emphasis on zoo-housed species.

Graphical Abstract

1. Introduction

Ticks (Acari: Ixodidae) are arthropod ectoparasites, distributed worldwide. They are strictly hematophagous and feed on numerous terrestrial vertebrate species, including mammals, reptiles, birds and amphibians [1]. Studies suggest that, on a local scale, host selection of ticks and other ectoparasites is connected mainly with the ecological habitat they occupy [2,3,4]. Even though ticks are highly adaptable and able to colonize various habitats, they are usually recognized (mainly among the public) as parasites typically found in rural or forest areas. This notion is contradicted by several recent studies which showed that ticks are also frequently observed in urban and peri-urban habitats [5,6,7,8]. Typical urban areas inhabited by ticks include recreational areas, parks and cemeteries [9,10,11]. The increasing rate of urbanization worldwide facilitates the creation of ecotones which are ideal for the emergence of hotspots of tick-borne pathogens (TBPs) that might infect free-living, domesticated and possibly even zoo-housed animal species, potentially also endangering the urban human population [12,13,14]. Zoological gardens (zoos) are popular urban recreational areas with a semiforested or park-like character. The seminatural, fragmented environment characteristic for zoos is created to host various animal species with different habitat requirements. This is a factor that positively influences the life cycle of ticks and other ectoparasites [15,16,17,18]. That is why zoos are nowadays recognized as potential TBPs refugia [19,20,21,22]. Animal species kept in such refugia can therefore potentially serve as tick and TBPs reservoirs, allowing further propagation of TBPs within their local ecosystems.
Indeed, several indigenous tick species have been reported in the areas of zoos, wildlife parks or farms worldwide. In the United States of America (USA) and Canada, Ixodes pacificus [23], Ixodes scapularis [24,25,26], Amblyomma americanum, Rhipicephalus sanguineus and Dermacentor variabilis [25,27,28] have been reported to exist in such captive exotic animal facilities. In Southern America, Brazilian zoo-animal infection cases have been connected to the following tick species of the Amblyomma and Rhipicephalus genera: A. dubitatum, A. calcaratum, A. aureolatum, A. sculptum or R. sanguineus in Southeastern regions of Brazil [21]. More Amblyomma species were collected from animals kept in zoos located in Northern and Northwestern Brazil: A. dissimile, A. variatum, A. geayi, A. longirostre, A. goeldii, A. humerale, A. naponense or A. nodosum [29,30]. In Europe, Ixodes ricinus is the most common tick found in zoos and wildlife parks or farms [20,31,32,33,34]. Nonindigenous tick species have been reported to feed on zoo animals, for example, the Asian tick, Amblyomma javanense, has been found on zoo-kept Asian water monitor (Varanus salvator) in South Carolina, USA [25].
All tick species belonging to the tick genera mentioned above (Amblyomma, Dermacentor, Ixodes and Rhipicephalus) develop in the three-host life cycle. The three-host life cycle is characteristic in its variability of host selection for each tick developmental stage (larvae, nymph and adult) [12]. Generally, the selection of natural hosts depends strongly on the development stage, in part due to different questing strategies connected to the position of the ticks on vegetation (how high each development stage can climb) [35]. Ideal hosts for tick larvae include small rodents like mice (for example Peromyscus spp. [36], Apodemus spp. [37]) or voles (for example Myodes spp. and Microtus spp. [37]), reptiles (like Bothrops spp. or Dispas spp. in Brazil [38]) and birds (for example migratory species like Anthus trivialis in Europe [39] or Melospiza melodia in the USA [40]). Such hosts are also suitable for nymphs. Both nymphs and larvae can also be found on larger animals like sheep, goats or other medium-sized animals [41,42]. Adult ticks frequently feed on larger animals, e.g., species of the Cervidae, Bovidae or Suidae families [35,42]. With each blood meal, ticks can acquire or spread various TBPs either by horizontal (stage-to-stage) transmission, vertical (female-to-egg) transmission or by cofeeding (nonsystemic) transmission [12,43,44]. Natural foci with the potential for emergence of TBPs represent a danger that is supported further by the ability of ticks and TBPs to adapt to host and habitat change [3,4,45,46].

2. Tick-Borne Pathogens in Zoo-Housed Animals

Infections caused by numerous TBPs have been reported in exotic (and local) animals under captive care in zoos, ranches, private farms and other similar facilities in many parts of the world (Figure 1). The various tick species that are able to transmit pathogens and are found in such facilities generally have well-studied vector capacity and competence for pathogens of medical and veterinary importance. Such key information can provide us with information regarding the risk of zoo-housed or urban-dwelling animals contracting tick-borne infections in a given geographic region.
The tick species that belong to I. ricinus complex, which are predominant in Eurasian zoos and wildlife farms, i.e., I. ricinus and Ixodes persulcatus, are the primary vectors of Rickettsiales like Anaplasma phagocytophilum [47], tick-borne encephalitis virus (TBEV) [20,48,49], Bartonella spp., Francisella tularensis, multiple Borrelia spp. [20,49,50] and Babesia spp. [49,51]. The ticks commonly found in North American and Canadian zoos or ranches, i.e., I. scapularis and I. pacificus, are also recognized vectors of dangerous pathogens. Both I. scapularis and I. pacificus are known to transmit spirochetes from Borrelia burgdorferi sensu lato complex and Borrelia myamotoi [50], Babesia microti, A. phagocytophilum, Ehrlichia muris-like sp. or deer tick virus [52]. A. americanum and D. variabilis ticks are known vectors of Cytauxzoon felis [53]. A. americanum is also known vector of Ehrlichia chaffeensis [54], Ehrlichia ewingii [55], Rickettsia amblyommii and Borrelia lonestari [56]. D. variabilis transmits Rickettsia rickettsii - causative agent of Rocky Mountain spotted fever and other Rickettsiales [57]. R. sanquineus, found in Southern and Northern American zoos, were confirmed to transmit Anaplasma platys, Hepatozoon canis, Cercopithifilaria spp. [58,59,60], Ehrlichia canis, Rickettsia massiliae, Rickettsia conorii and R. rickettsii [59,60]. The majority of tick species found on animals housed in zoos and botanical gardens of Southern America, Brazil in particular, belong to the genus Amblyomma. In the Northern regions of Brazil A. geayi, A. varium, A. longirostre have been confirmed as vectors of Rickttsia amblyommatis [29,61,62,63,64]. A. varium, A. nodosum and A. humerale are able to transmit Rickettsia bellii [29,62,63,64,65]. A. dissimile was confirmed to carry Rickettsia sp. of the colombianensi strain [29,66], A. nodosum is also able to carry Rickettsia parkeri-like agent [29,65]. Further studies confirmed the presence of A. sculptum and A. aureolatum the main vectors of R. rickettsii (Brazilian spotted fever) in Southern regions of Brazil [21,67]. Other released results revealed the ability of A. calcaratum to vector the NOD strain of Rickettsia sp. [68] while A. dubitatum was confirmed to transmit several Rickettsia sp. [69] (see Figure 1 for an overview of the various tick species and their natural geographical distribution). These findings reveal the heightened risk for captive wildlife animals to be infected with the aforementioned pathogens. The risk of infection, however, is influenced by a large spectrum of factors including the reservoir capacity of the infected animal species or the presence of natural reservoir hosts of selected TBPs (for example, i.e. Peromyscus leucopus) that are able to thrive in urban environment [70]. The clinical manifestation of tick-borne diseases (TBDs) depends on the infected animal species; they can be hidden and nonspecific, which leads to underestimates of the epizootiology and pathology of many TBDs and their related issues among captive wildlife species. However, there are also reports of infections of tick-borne pathogens which have led to serious diseases and even fatalities, as will be discussed in this review.

3. Tick-Borne Encephalitis Virus (TBEV)

The TBEV can infect a wide range of mammals [71]. In humans, nonhuman primates, dogs and some rodent species, it can cause serious, and sometimes fatal, meningoencephalitis [72,73,74]. In ungulates, TBEV usually causes a subclinical infection, but the virus can be excreted into the milk of viremic individuals [75]. In rodents and insectivores, TBEV infection leads to long viremia without symptoms; this makes such species suitable reservoirs for the virus [71,76,77].
In 2006, a fatal case of TBEV infection was described in a female Barbary macaque (Macaca sylvanus) kept within the monkey enclosure of a zoo situated in southern Germany [78]. The monkey suffered staggering paresis of the hindlegs, incoordination and intermittent opisthotonos, before entering a coma four days after the onset of these symptoms. The comatose monkey was subsequently euthanized, and a post mortem necropsy, polymerase chain reaction (PCR) tests and histological tests confirmed an infection with TBEV. Even though this was the first described case of a natural TBEV infection in macaques, it was very similar to experimental infections of macaques used as model organisms for TBEV pathogenesis [78,79]. Later, serological tests were conducted on the remaining 283 macaques living within the same enclosure; among them, six (2.1%) were seropositive for anti-TBEV antibodies [72]. Anti-TBEV antibodies were also detected in sheep on the neighboring pastures, with a seroprevalence of 9% [72]. Similar cases could be prevented in the future, as macaques (and probably other primates) are likely to develop anti-TBEV immunity after vaccination with TBEV vaccines designed for human-use [80].
On the other hand, tests for anti-TBEV antibodies among other zoo animals were mostly negative, according to previous Czech zoological research results [20]. In this research, only two seropositive samples were recorded out of 133 tested serum samples from 69 animal species: one from a markhor (Capra falconeri) and one from a reindeer (Rangifer tarandus), as confirmed by both enzyme-linked immunosorbent assay and a neutralization test.

4. Lyme Borreliosis Spirochetes

Lyme borreliosis (LB) spirochetes can cause systemic disease in humans, nonhuman primates, carnivores, ungulates and some rodent species [81,82,83], causing pathological changes in the skin, joints, heart and central nervous system [84,85]. However, clinical symptoms of LB in different animal species are variable [86,87]. They are influenced by, among other factors, the species of the Borrelia species and strain [88,89,90], as well as the host animal species and its breed. Different symptoms can be observed between horses [91,92], dogs [92,93,94] and natural hosts, like the white-footed mouse (P. leucopus) [90]. However, in many individuals, Borrelia infection symptoms are nonspecific, and asymptomatic infections are common in seropositive animals with lower antibody titers [87,91,94].
The prevalence of Borrelia among zoo animals has been investigated in Germany and the Czech Republic [19,20]. High numbers of Borrelia-infected individuals, or individuals having anti-Borrelia antibodies, were found in both studies. In the Czech Republic, DNA from spirochetes of the B. burgdorferi sensu lato complex was detected in a significant number of the tested vertebrate serum samples (69 positive cases, out of 133 tested samples – 51.8% affected). Those species with the highest number of positive samples were the Barbary sheep (Ammotragus lervia) with five positive samples (total sample size: n = 6), Grant’s zebra (Eguus quagga boehmi) also with five (n = 6), Hartmann’s mountain zebra (Equus zebra hartmannae) with four positive samples (n = 5), Grey wolves (Canis lupus) with four positives (n = 4) and Addax (Addax nasomaculatus) with five positive samples (n = 5) (Table 1; [20]). In Germany, sera from 1487 zoo animals were tested for the presence of anti-Borrelia antibodies. One hundred fifty-four samples (10.4%) were positive, while 168 samples (11.3%) produced borderline results. The highest number of positive samples was observed in Przewalski horses (Equus przewalskii), with 22 positives out of 98 tested animals, lions (Panthera leo), where 11 out of the 49 tested lions were positive, and forest buffalo (Syncerus caffer nanus), where four out of nine were positive ([19]; Table 1). Considering these studies [19,20,22], it is obvious that several animal species are susceptible to Borrelia infection. Among these are also the domestic goat (Capra aegagrus f. hircus), Barbary sheep (A. lervia), markhor (C. falconeri), mountain goat (Oreamnos americanus) and llama (Lama guanicoe) (Table 1). However, in some cases, the results of these studies varied. For example, in the German study, significant numbers of positive sera samples were found in domestic cattle (Bos primigenius f. taurus) and impala (Aepyceros melampus) [19]; however, in the Czech study, the sera of these animal species were negative [20]. On the other hand, the opposite was true for African wild dogs (Lycaon pictus) within the two zoos [19,20].
The serum complement of some animal species has a borreliacidal effect, which not only protects these animals from spirochete infection, but also purges Borrelia from infected ticks feeding on these animals [22,95,96]. This has a strong impact on the ecology of LB spirochetes within ecosystems where such animals are present.
In research conducted by Ticha et al. [22], serum samples from zoo animals were tested for possible borreliacidal effects on three species of spirochetes from the B. burgdorferi sensu lato complex (B. burgdorferi sensu stricto (s.s.), Borrelia garinii and Borrelia afzelii). From the 135 tested serum samples from various zoo animals, 78 demonstrated some borreliacidal effect towards at least one of the tested Borrelia spp. The strongest borreliacidal effect was observed in the sera from the Burmese python (Python bivittatus), European rabbit (Oryctolagus cuniculus), radiated tortoise (Astrochelys radiata) and impala (A. melampus) (Table 1). Of all of the tested sera, only some showed borreliacidal effects toward all three tested Borrelia spp., as showed in Table 1. Most samples possessed selected resistance (resistance only towards one or two of the tested Borrelia types) or were sensitive to the studied Borrelia species. Sera from most of the carnivores, even-toed ungulates, rodents and some reptiles, showed only weak borreliacidal effects on the tested spirochetes.
The absence of a borreliacidal effect in the sera of some zoo animals could be an indication of their permissiveness to Borrelia infections, suggesting that these animals can theoretically serve as Borrelia reservoirs. On the other hand, animals whose sera have strong borreliacidal effects should be resistant to Borrelia infection. Unfortunately, no tests were conducted to assess whether these animals could also resolve Borrelia in the infected ticks feeding on them.

5. Babesia, Theileria and Cytauxzoon Piroplasmida

Babesia species are often observed in captive or semicaptive cervids and bovids [24,34,97,98,99], but they have also been found in other captive animal species. These protozoan parasites can complete their life cycle within multiple tick species, including I. scapularis [98,99], I. ricinus [97,100], Dermacentor albipictus [101], A. americanum [24] and I. pacificus [99]. Babesiosis has a range of typical symptoms, like hemolytic anemia, jaundice, fever, shaking and hemoglobinuria [102]. However, an asymptomatic disease course is also possible, especially in animals with a well-developed immunity [98].
Cases of acute babesiosis in nonindigenous cervids were reported in 2009 and 2012 in Germany [34]. In response, a nation-wide project was conducted in 2013, where samples were collected from 16 zoos located across the country [34]. This survey resulted in the detection of Babesia capreoli, Babesia divergens, Babesia venatorum, Theileria spp. and one unidentifiable Babesia sp., in captive reindeer (R. tarandus). Of the 123 tested reindeer samples, 29 were positive (23.6%), and 12 of the 16 facilities harbored at least one reindeer that tested positive for Babesia spp. [34].
Other babesiosis outbreaks were recorded in the Netherlands in 2011 and 2015 [97,103]. In 2011, a captive-bred forest reindeer calf died due to an acute B. venatorum infection [103]. In 2015, five out of 14 reindeer kept in the Ouwehand Zoo tested positive for B. capreoli, either through PCR testing or blood smears. Of the five positive animals, two died, one was euthanized and another animal died without testing positive for Babesia spp. All the mortalities were among young calves, born in the year of the outbreak, or in 2014. The surviving individuals with positive test results were adult females with no clinical signs of disease [97]. In Switzerland, a case report was published in 2019 identifying a young, captive reindeer calf with severe babesiosis infection clinical signs as positive for B. venatorum [32]. In Great Britain, seven fatal cases of babesiosis were confirmed in captive reindeer between the years 1997 and 1998, and B. divergens was identified as the probable causative species [104].
Canada and USA have also reported several acute and subclinical cases of babesiosis. Two fatal cases were reported in Canada in 2012, involving Babesia spp. isolated from captive-bred adult wapiti (Cervus canadensis) [105]. Between the years 2013 and 2016, nine fatal babesiosis cases were detected in Canadian zoo-kept adult reindeer and wapiti [24]. A higher number of positive cases were observed in Canada between the years 2016 to 2018 in zoo, or farm-kept cervids, like wapiti and red deer (Cervus elaphus) [98]. In the USA, fatal babesiosis infections were described very early in captive-bred cervids, including in caribou (Rangifer tarandus caribou) at the Minnesota Zoo [106] and the North American elk (Cervus elaphus canadiensis) kept on a farm in Texas [101]. Other severe American cases of babesiosis were observed in 2003 (semicaptive, adult North American elk; [107]) and in 2005 (adult captive reindeer from New York zoo; [108]). The study from New York zoo also identified three asymptomatic hosts of B. odocoilei: Yak (Bos grunniens), muntjac (Muntiacus reevesi) and markhor (C. falconeri) [108].
All the aforementioned Canadian and American studies related the positive samples to Babesia odocoilei. This Babesia species seems to be predominant in Canadian and North American captive cervids [24,98,105,107]. Considering these cases, it can be reasonably assumed that babesiosis is yet another global, tick-borne related threat to captive cervids.
However, babesiosis infection is not exclusive to cervids and bovids; research conducted in several Brazilian zoos showed the prevalence of babesiosis in zoo felids, canids and a genet (Genetta tigrina). Most animals were seropositive for Babesia canis, but some (Oncifelis colocolo and the genet) were positive for a Babesia sp. with close similarity to Babesia leo, according to DNA testing [109]. In addition, free-roaming domestic cats in Brazil often stray into zoo areas and are therefore considered potential carriers of babesiosis. Both Babesia sp. (Babesia vogeli) and Theileria sp. were confirmed in some of the tested cat samples in the same area as these Brazilian zoo animals [110]. In Kansas, USA, an unknown Babesia spp. was observed in maned wolves (Chrysocyon brachyurus) in 2012 (first occurrence) and again in 2019. Both cases had severe clinical symptoms, and one case (2012) was fatal, even after treatment [111,112].
Piroplasms of the genera Theileria and Cytauxzoon are also dangerous protozoan parasites. Theileria have been observed in many tick species, including Amblyomma spp., Haemahysalis spp., Rhipicephalus spp. and Hyalomma spp. [113], whereas Cytauxzoon has been found in Dermacentor spp. [113,114,115]. Theileria species are variable in their pathogenesis and lifecycles; there are the so-called “transforming” species (T. annulata, T. parva, T. lestoquardi, T. taurotragi etc.) and the “nontransforming” species (T. orientalis, T. mutans, T. cervi and T. velifera) [113,116,117]. The transforming Theileria species have the ability to influence host leucocytes, causing them to enable unlimited proliferation of infected cells [116], resulting in symptoms such as polyphagia followed by anorexia, nasal discharge, fever, anemia, febrile generalized lymphadenopathy and hemorrhaging on the mucous membranes of the buccal cavity and conjunctiva [113,118]. Such an infection may be fatal. The nontransforming species lack the ability to cause proliferation, resulting mostly in benign infections with mild symptoms [116]. These symptoms can become chronic, causing anemia or persistent subclinical infections [119]. Theileria infections vary in terms of symptoms, depending on the infected animal species and the Theileria species. Besides from the free-roaming cats of Brazil [110], an unknown Theileria spp. was detected in Missouri, USA, in an adult male captive reindeer (R. tarandus [120]). Infections of South American tapirs (Tapirus terrestris) with Theileria equi were confirmed in zoo and botanical gardens located in Northern parts of Brazil [121]. Theileria bicornis was detected in samples of captive white rhinoceros (Ceratotherium simum) and black rhinoceros (Diceros bicornis) in Australian zoo [117]. A Theileria spp. was also found in the blood sample of one captive reindeer (R. tarandus) kept in a German zoo [34].
Cytauxzoon felis is a parasite of felids, of both wild and domestic origin. This parasite has been observed on several occasions in samples from zoo felids reared in Brazil, i.e., in ocelots (Leopardus pardalis) [114,122], lions (P. leo) [115], pumas (Puma concolor) and jaguars (Panthera onca) [114]. In Florida, USA, a white tiger (Panthera tigris) housed in a private breeding facility was also reported as positive for C. felis [123]. Cytauxzoonosis infection can be asymptomatic [114], but also fatal [115,123]. The disease has two phases: erythrocytic and macrophagic [124]. The erythrocytic phase is usually connected to anemia, while the macrophagic phase is marked by systemic circulatory obstructions, caused by schizont macrophages, and presents clinical signs such as anorexia, depression, dehydration, fever, icterus and dyspnea [124,125].

6. Rickettsiales

The bacteria of the order Rickettsiales cause a variety of diseases of veterinary and medical importance, including bovine anaplasmosis, human ehrlichiosis, Rocky Mountain spotted fever and scrub typhus [126]. Within the order Rickettsiales, the genera Rickettsia, Ehrlichia and Anaplasma are dependent on tick vectors like A. americanum, R. sanguineus, D. variabilis, Ixodes spp., Haemaphysalis spp., Hyalomma spp. and Aponomma spp. [23,26,28,31,127,128]. Various, and often nonspecific, clinical symptoms are associated with Rickettsiales infections in animals (anorexia, depression, dehydration, fever, lethargy, lymphadenopathy and ataxia) [23,26,28,129]. Acute infections with bacteria from the Anaplasmataceae family (Anaplasma, Ehrlichia) can be detected using blood smears, showing a characteristic “morulae” (mulberry-shaped microcolonies) located in the host cell cytoplasm [26,28,128].
In Europe, several reports have confirmed positive cases for Rickettsiales. A. phagocytophilum has been found in blood samples of captive reindeer (R. tarandus) kept in German zoos [33]. Furthermore, an asymptomatic lion (P. leo) was positive for an infection with Rickettsia sp. and A. phagocytophilum in Italy [130]. Acute anaplasmosis (A. phagocytophilum) was observed in captive timber wolves (Canis lupus occidentalis) in Austria [31].
In the USA, several cases were also reported for anaplasmosis (A. phagocytophilum), in four captive Przewalski’s horses (E. przewalskii) from Virginia [26]. E. chaffeensis was found in five ring-tailed lemurs (Lemur catta) and one ruffed lemur (Varecia variegate rubra) in the Duke Lemur Center in North Carolina (USA; [28]). A. phagocytophilum (under the old nomenclature of Ehrlichia equi in the case report) was confirmed in llama (Lama glama) from California, USA [23] and lastly, canine ehrlichiosis was noted in Florida, USA, in wolves, dogs and wolf-dog crosses [27].
Substantial research from Brazilian zoos showed that Ehrlichia canis was found in the following captive felids: jaguars (P. onca), ocelots (L. pardalis), jaguarundi (Puma yagouaroundi) and little spotted cats (Leopardus tigrinus). In this research, antibodies were found in four felids: two jaguarundi, one little spotted cat and one margay (Leopardus wiedii; [131]). Another study from Brazil confirmed that antibodies for E. canis existed in captive ocelots [122]. Further studies from André et al. [132] confirmed Ehrlichia spp. in captive canids, including European wolves (C. lupus), bush dogs (Speothos venaticus) and crab-eating foxes (Cerdocyon thous). Pumas (P. concolor), little spotted cats (L. tigrinus), ocelots (L. pardalis), jaguarundis (P. yagouaroundi), tigers (P. tigris) and lions (P. leo) also tested positive for Ehrlichia spp. Furthermore, Anaplasma spp. was confirmed in bush dogs and little spotted cats [132]. Three free-roaming cats surrounding the Brazilian zoo also tested positive for Anaplasma spp., which is closely related to A. phagocytophilum [110], showing that local animals can be a source of tick-borne pathogens that are then transferred to zoo-kept animals.

7. Coinfections with Multiple and Less Common Pathogens

In a report of Zhang et al. [133], novel Theileria spp., together with A. phagocytophilum and Anaplasma bovis, were found in the post mortem dissection of a one-year old South African giraffe (Giraffa camelopardalis giraffa), which was kept in Zhengzhou Zoo, China. The animal died suddenly, one day after the onset of severe clinical symptoms [133]. Another coinfection was observed in a lion (P. leo) in the Fasano Safari park in Italy. The animal tested positive for Coxiella burnetii, Rickettsia sp. and A. phagocytophilum [130]. In 2017, a rare emerging tick-borne virus causing severe fever and thrombocytopenia syndrome phlebovirus (SFTSV) was identified in two fatal cases in cheetah, infected in Hiroshima City Asa Zoological Park, Japan [134].
Regarding the aforementioned TBPs in zoo-housed and captive animals, Table 2 summarizes the prevalence, country of origin, animal species and collected tick species (excluding Borrelia spp. since these are discussed extensively in Table 1)

8. Conclusions and Recommendations

All of the aforementioned studies confirm the significant threat of ticks and tick-borne diseases to wild animals housed in zoos, wildlife parks or farms. Such zoo and zoo-like areas have been identified as being suitable for tick vectors and reservoir hosts of TBPs. The pathogens found in zoo-housed animals included viruses (TBEV, SFTSV), bacteria (Borrelia, Anaplasma, Ehrlichia, Rickettsia spp.) and protozoal parasites (Babesia, Cytauxzoon and Theileria spp.). It was confirmed that infection of the tick vectors with some of these pathogens, for example, Borrelia spp., TBEV, Anaplasma spp. and Babesia spp., increases the tick mobility, cold resistance, desiccation resistance and overall chance of survival [135]. There are other known tick-borne threats that are yet to be observed in zoo-housed animals, like the filariid nematode species Cercopithifilaria spp. and Acanthocheilonema spp. These parasites are frequently associated with dogs [136,137,138,139,140] and occasionally with wild-living animals [141]. They can be transmitted by various tick species, i.e., Haemaphysalis flava, Haemaphysalis japonica [141], A. americanum [142], I. scapularis [143,144] and R. sanquineus [145,146]. Focused sampling should be conducted to determine the potential spread of these parasites in zoos and other similar establishments.
Clinical manifestations of infections with the TBPs in captive animals can vary from unapparent to serious and even life threating [147]. It is clear that captive animals have variable sensitivities to the studied pathogens; however, it is not clear if zoo and farm-housed animals play a significant role as tick hosts and TBP reservoirs in their ecosystems. In the case of TBPs, most of them are probably incidental dead-end hosts, as they would not produce sufficient bacteremia/viremia for the infection of other ticks (although this question remains to be answered definitively). Figure 2 provides a summary of the amount of samples collected and tested across the several orders of zoo-housed animals (with connection to TBPs). More abundant sampling (Artiodactyla, Carnivora,) provides results that can be used to evaluate the role of these animal orders in the ecology of several TBPs. Data on Primates and Preissodactyla are insufficient to draw any wider conclusions in terms of overall TBP transmission, and they usually provide information about the incidence of only one pathogen (case reports).
Some of the pathogens (TBEV, Borrelia spp., A. phagocytophilum, E. cheffeensis, C. burnetii) and tick species (A. americanum, A. sculptum I. ricinus, I. scapularis, D. variabilis) detected in zoos or zoo-like areas represent a notable threat to the health of humans that live nearby. Since zoos are places with high densities of humans, exotic animals, domestic animals and wildlife opportunists, they create ideal hotspots for the spread of TBPs, ticks and other ectoparasites [18]. The importance of surveillance and research of tick vectors and TBPs that exist in close proximity to human habitats is supported by the fact that the annual number of visitors to zoos is more than 700 million worldwide [148]. The already available evidence of tick-borne pathogens infecting zoo-housed animals should raise awareness of scientists, zookeepers, veterinarians, medical doctors and other specialists.
Another risk for zoo and other captive animals is free-roaming domestic cats that often stray into zoo or farm grounds. These cats are commonly infested with local ticks, and are hosts to various vector-borne infections [110,149,150,151]. They can thus potentially serve as one of the sources that increase the numbers of infected ticks in the areas that they commonly occupy. As a preventative measure, the activity of free-roaming domestic cats should be monitored and minimized in establishments where exotic animals are kept. Advanced preventative techniques in the forms of various vaccines are also available for the prevention of tick-borne infections in some animal species. In addition to the existing TBEV vaccine approved for human use, which was shown to be efficient for other primates [80], there is a borrelia vaccine approved for use in dogs [152]. Recently, this vaccine was tested on horses [153], and it could be expected that it may trigger protection in other animals too, at the very least, in canids. Furthermore, vaccines against bovid ticks from the genus Rhipicephalus were developed for use in cattle [154], and since the vaccine works in sheep as well, it can be expected that it may protect other ruminant species [154]. Also, landscape management with respect to tick-associated risks can help lower the prevalence of ticks, and subsequently, of TBPs, thus enhancing any other preventative measures taken [155].
In conclusion, ticks and TBPs present a challenge for a wide range of zoo, veterinary and public health experts. However, due to the poor understanding of the role of zoo animals in the biology of ticks and TBPs, further research in this area is clearly urgently required.

9. Other Potentially Tick-Borne Threats to Zoo-Housed and Captive Animals

Some pathogens are less specialized and spread through a wider range of vectors, e.g., vertebrates, mites, lice, mosquitoes and, of course, ticks. Even though some pathogens are less studied, they still represent a threat to both animal and human health.
Bacteria of the order Chlamydiales have been connected to Ixodid ticks for some time [156,157,158,159]. The most intensively studied is the Chlamydiaceae family. Other families are included in the order, but they are usually summarized under the term Chlamydia-like organisms (CLOs). These bacterial pathogens are causative agents of wide range of human and animal (some zoonotic) diseases [160]. Tick-borne CLO transmissions have been observed in humans [156], while various species of animals have been confirmed to harbor chlamydial agents, but without the direct connection to ticks. Among vertebrates, several species of bats (free-living and captive) have been found to be positive for a wide range of CLOs [161]. Chlamydophila psittaci has been found in the eyes of various livestock [162]. Chlamydophila abortus and Chlamydophila pecorum has been detected in a water buffalo (Bubalus bubalis) [163]. Chlamydia felis infection has been confirmed in cats and dogs [164], while Chlamydiaceae has been detected in domestic pigs (Sus scrofa f. domestica) [165]. These studies suggest the possibility of infection for both humans and captive/domestic animals living in their close vicinity.
Another potentially tick-borne pathogen that causes health problems is the bacteria F. tularensis. This pathogen can be transmitted through various sources: aerosol droplets, infected animal carcasses, contaminated food (alimentary transmission) or the bite of an infected arthropod [166,167]. F. tularensis can be transmitted by all tick life stages and horizontal transmission has been confirmed [167]. There have been positive cases of tularemia infection in animals in several zoological gardens. A fatal case in a Bornean orangutan (Pongo pygmaeus) was reported at Topeka Zoo, Kansas in 2003 [25], which was directly connected to tick bite. Several other zoos in North America have confirmed F. tularensis infections in other animal species: golden-lion tamarins (Leontopithecus rosalia), red-handed tamarin (Saguinus midas) [25], squirrel monkeys (genus Saimiri) [168], black and white-ruffed lemurs (Varecia variegate), ring-tailed lemurs (L. catta), white handed gibbon (Hylobates lar) and greater spotnose guenon (Cercopithecus nictitans) [169]. F. tularensis infections have also been observed in animals in German zoos (in a wide range of animal species) [170]. Human and animal (tamarins and a talapoin monkey (Miopithecus talapoin)) cases have also been reported in Canada [171]. However, none of these studies provided any link to tick or other ectoparasite bites, so it remains unclear whether the connection exists. Nonetheless, it is still evident that zoo-housed animals and humans are threatened by this pathogen.
Bacteria of the genus Bartonella are known to cause various diseases, for example, the cat scratch disease in humans [172]. Bartonella spp. has been connected to several tick species [172,173,174,175]. Domestic cats are known reservoirs of Bartonella spp., e.g., B. henselae, B. clarridgeiae and B. koehlerae [176,177]. Samples from free-roaming domestic cats located in zoo areas in Brazil have been found to be positive for Bartonella spp. [110]. This could lead to spillover of this pathogen to the zoo tick population, even though the described infestation was most likely flea-borne [110]. Recently, tick-borne Bartonella spp. cases have been observed in dromedary camels (Camelus dromedarius) infected with B. henselae [178], domesticated yaks (Bos grunniens) [179] and in livestock animals like cattle [180,181], goats [181,182] and horses [182]. Some of these species, like dromedary camels or yaks, are often kept in zoos, so this information may be useful for the prevention of this potentially tick-borne disease.
There are other widely known pathogens that are yet to be fully established as potentially tick-borne, e.g., the parasite Toxoplasma gondii. Even though this parasite is not usually associated with ticks, some studies have proved the ability of ticks to transmit it [183,184]. In conclusion, it should be noted even pathogens which are less commonly attributed to ticks and captive animals have the potential to cause serious damage.

Author Contributions

Conceptualization, J.H., N.R. and J.Č.; methodology, J.H.; validation, J.H., J.Č., I.S. and N.R.; formal analysis, J.H.; investigation, J.H., I.S.; resources, L.G., N.R. and M.G.; data curation, J.H.; writing—original draft preparation, J.H.; writing—review and editing, J.H., I.S., N.R., L.G., M.G. and J.Č.; visualization, J.H.; supervision, N.R., J.Č. and I.S.; project administration, J.Č., N.R., M.G. and L.G.; funding acquisition, J.Č., N.R. and L.G. All authors have read and agreed to the published version of the manuscript.


This research was funded by NÁRODNÍ AGENTURA PRO ZEMĚDĚLSKÝ VÝZKUM, grant number QK1920258 and by ČESKÁ ZEMĚDĚLSKÁ UNIVERZITA, grant number 20205013. The APC was funded by QK1920258.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

No new data were created or analyzed in this study. Data sharing is not applicable to this article.


The authors would like to thank all colleagues from Czech University of Life Sciences and Biology Centre in Budweis, for their contributions towards this review paper. We would also like to thank Tersia Needham, representing the company “Science Unleashed” for the English text corrections.

Conflicts of Interest

The authors declare no conflict of interest.


  1. Sonenshine, D.E.; Roe, R.M. (Eds.) Biology of Ticks Volume 1, 2nd ed.; Oxford University Press: Oxford, UK, 2014; pp. 4–8. [Google Scholar]
  2. Krasnov, B.R.; Mouillot, D.; Shenbrot, G.I.; Khokhlova, I.S.; Vinarski, M.V.; Korallo-Vinarskaya, N.P.; Poulin, R. Similarity in Ectoparasite Faunas of Palaearctic Rodents as a Function of Host Phylogenetic, Geographic or Environmental Distances: Which Matters the Most? Int. J. Parasitol. 2010, 40, 807–817. [Google Scholar] [CrossRef]
  3. McCoy, K.D.; Léger, E.; Dietrich, M. Host Specialization in Ticks and Transmission of Tick-Borne Diseases: A Review. Front. Cell. Infect. Microbiol. 2013, 3. [Google Scholar] [CrossRef] [Green Version]
  4. Jia, N.; Wang, J.; Shi, W.; Du, L.; Sun, Y.; Zhan, W.; Jiang, J.-F.; Wang, Q.; Zhang, B.; Ji, P.; et al. Large-Scale Comparative Analyses of Tick Genomes Elucidate Their Genetic Diversity and Vector Capacities. Cell 2020, 182, 1328–1340.e13. [Google Scholar] [CrossRef]
  5. Hansford, K.M.; Fonville, M.; Gillingham, E.L.; Coipan, E.C.; Pietzsch, M.E.; Krawczyk, A.I.; Vaux, A.G.C.; Cull, B.; Sprong, H.; Medlock, J.M. Ticks and Borrelia in Urban and Peri-Urban Green Space Habitats in a City in Southern England. Ticks Tick-Borne Dis. 2017, 8, 353–361. [Google Scholar] [CrossRef]
  6. Lindquist, L. Recent and Historical Trends in the Epidemiology of Japanese Encephalitis and Its Implication for Risk Assessment in Travellers. J. Travel Med. 2018, 25, tay006. [Google Scholar] [CrossRef] [Green Version]
  7. Lydecker, H.W.; Hochuli, D.F.; Banks, P.B. Peri-Urban Black Rats Host a Rich Assembly of Ticks and Healthier Rats Have More Ticks. Ticks Tick-Borne Dis. 2019, 10, 749–753. [Google Scholar] [CrossRef]
  8. Sormunen, J.J.; Kulha, N.; Klemola, T.; Mäkelä, S.; Vesilahti, E.-M.; Vesterinen, E.J. Enhanced Threat of Tick-Borne Infections within Cities? Assessing Public Health Risks Due to Ticks in Urban Green Spaces in Helsinki, Finland. Zoonoses Public Health 2020, 67, 823–839. [Google Scholar] [CrossRef]
  9. Cicuttin, G.L.; De Salvo, M.N.; Venzal, J.M.; Nava, S. Borrelia Spp. in Ticks and Birds from a Protected Urban Area in Buenos Aires City, Argentina. Ticks Tick-Borne Dis. 2019, 10, 101282. [Google Scholar] [CrossRef]
  10. Heylen, D.; Lasters, R.; Adriaensen, F.; Fonville, M.; Sprong, H.; Matthysen, E. Ticks and Tick-Borne Diseases in the City: Role of Landscape Connectivity and Green Space Characteristics in a Metropolitan Area. Sci. Total Environ. 2019, 670, 941–949. [Google Scholar] [CrossRef]
  11. Klemola, T.; Sormunen, J.J.; Mojzer, J.; Mäkelä, S.; Vesterinen, E.J. High Tick Abundance and Diversity of Tick-Borne Pathogens in a Finnish City. Urban Ecosyst. 2019, 22, 817–826. [Google Scholar] [CrossRef] [Green Version]
  12. Estrada-Peña, A.; de la Fuente, J. The Ecology of Ticks and Epidemiology of Tick-Borne Viral Diseases. Antivir. Res. 2014, 108, 104–128. [Google Scholar] [CrossRef] [PubMed]
  13. Millán, J.; Proboste, T.; Fernández de Mera, I.G.; Chirife, A.D.; de la Fuente, J.; Altet, L. Molecular Detection of Vector-Borne Pathogens in Wild and Domestic Carnivores and Their Ticks at the Human–Wildlife Interface. Ticks Tick-Borne Dis. 2016, 7, 284–290. [Google Scholar] [CrossRef]
  14. Swei, A.; Couper, L.I.; Coffey, L.L.; Kapan, D.; Bennett, S. Patterns, Drivers, and Challenges of Vector-Borne Disease Emergence. Vector-Borne Zoonotic Dis. 2019, 20, 159–170. [Google Scholar] [CrossRef] [PubMed]
  15. Kazimírová, M.; Hamšíková, Z.; Kocianová, E.; Marini, G.; Mojšová, M.; Mahríková, L.; Berthová, L.; Slovák, M.; Rosá, R. Relative Density of Host-Seeking Ticks in Different Habitat Types of South-Western Slovakia. Exp. Appl. Acarol. 2016, 69, 205–224. [Google Scholar] [CrossRef]
  16. Diuk-Wasser, M.A.; VanAcker, M.C.; Fernandez, M.P. Impact of Land Use Changes and Habitat Fragmentation on the Eco-Epidemiology of Tick-Borne Diseases. J. Med. Entomol. 2020. [Google Scholar] [CrossRef]
  17. Froeschke, G.; van der Mescht, L.; McGeoch, M.; Matthee, S. Life History Strategy Influences Parasite Responses to Habitat Fragmentation. Int. J. Parasitol. 2013, 43, 1109–1118. [Google Scholar] [CrossRef]
  18. Adler, P.H.; Tuten, H.C.; Nelder, M.P. Arthropods of Medicoveterinary Importance in Zoos. Annu. Rev. Entomol. 2011, 56, 123–142. [Google Scholar] [CrossRef]
  19. Stoebel, K.; Schoenberg, A.; Streich, W.J. The Seroepidemiology of Lyme Borreliosis in Zoo Animals in Germany. Epidemiol. Infect. 2003, 131, 975–983. [Google Scholar] [CrossRef] [PubMed]
  20. Širmarová, J.; Tichá, L.; Golovchenko, M.; Salát, J.; Grubhoffer, L.; Rudenko, N.; Nowotny, N.; Růžek, D. Seroprevalence of Borrelia Burgdorferi Sensu Lato and Tick-Borne Encephalitis Virus in Zoo Animal Species in the Czech Republic. Ticks Tick-Borne Dis. 2014, 5, 523–527. [Google Scholar] [CrossRef]
  21. Gonzalez, I.H.L.; Labruna, M.B.; Chagas, C.R.F.; Salgado, P.A.B.; Monticelli, C.; Morais, L.H.; de Moraes, A.A.; Antunes, T.C.; Ramos, P.L.; Martins, T.F. Ticks Infesting Captive and Free-Roaming Wild Animal Species at the São Paulo Zoo, São Paulo, Brazil. Rev. Bras. Parasitol. Veterinária 2017, 26, 496–499. [Google Scholar] [CrossRef] [Green Version]
  22. Ticha, L.; Golovchenko, M.; Oliver, J.H.; Grubhoffer, L.; Rudenko, N. Sensitivity of Lyme Borreliosis Spirochetes to Serum Complement of Regular Zoo Animals: Potential Reservoir Competence of Some Exotic Vertebrates. Vector-Borne Zoonotic Dis. 2016, 16, 13–19. [Google Scholar] [CrossRef]
  23. Barlough, J.E.; Madigan, J.E.; Turoff, D.R.; Clover, J.R.; Shelly, S.M.; Dumler, J.S. An Ehrlichia Strain from a Llama (Lama Glama) and Llama-Associated Ticks (Ixodes Pacificus). J. Clin. Microbiol. 1997, 35, 1005–1007. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  24. Mathieu, A.; Pastor, A.R.; Berkvens, C.N.; Gara-Boivin, C.; Hébert, M.; Léveillé, A.N.; Barta, J.R.; Smith, D.A. Babesia Odocoilei as a Cause of Mortality in Captive Cervids in Canada. Can. Vet. J. 2018, 59, 52–58. [Google Scholar]
  25. Nelder, M.P.; Reeves, W.K.; Adler, P.H.; Wozniak, A.; Wills, W. Ectoparasites and Associated Pathogens of Free-Roaming and Captive Animals in Zoos of South Carolina. Vector-Borne Zoonotic Dis. 2009, 9, 469–477. [Google Scholar] [CrossRef] [PubMed]
  26. Sim, R.R.; Joyner, P.H.; Padilla, L.R.; Anikis, P.; Aitken-Palmer, C. Clinical Disease Associated with Anaplasma Phagocytophilum Infection in Captive Przewalski’s Horses (Equus Ferus Przewalskii). J. Zoo Wildl. Med. 2017, 48, 497–505. [Google Scholar] [CrossRef] [PubMed]
  27. Harvey, J.W.; Simpson, C.F.; Gaskin, J.M.; Sameck, J.H. Ehrlichiosis in Wolves, Dogs, and Wolf-Dog Crosses. J. Am. Vet. Med. Assoc. 1979, 175, 901–905. [Google Scholar]
  28. Williams, C.V.; Steenhouse, J.L.V.; Bradley, J.M.; Hancock, S.I.; Hegarty, B.C.; Breitschwerdt, E.B. Naturally Occurring Ehrlichia Chaffeensis Infection in Two Prosimian Primate Species: Ring-Tailed Lemurs (Lemur Catta) and Ruffed Lemurs (Varecia Variegata)-Volume 8, Number 12—December 2002-Emerging Infectious Diseases Journal-CDC. Emerg. Infect. Dis. 2002, 8, 12. [Google Scholar] [CrossRef]
  29. Nascimento, K.K.G.D.; Veríssimo, S.M.M.; Raia, V.D.A.; Guimarães, R.C.S.; Seade, G.C.C.; Azevedo, A.C.P.; Matos, S.P.; Oliveira, J.M.D.; Bezerra, I.A.; Martins, T.F.; et al. Tick Fauna of Wild Animals Received and Attended at the Santarém Zoological Park, Western Pará State, Brazil. Ciênc. Rural 2017, 47. [Google Scholar] [CrossRef] [Green Version]
  30. Souza, S.F.; Medeiros, L.S.; Oliveira, R.S.; Deschk, M.; Carvalho, Y.K.; Ribeiro, V.M.F.; Souza, A.P.; Lavina, M.S. Primeiro registro de Amblyomma geayi (Acari: Ixodidae) em preguiça (Bradypus variegatus) no estado do Acre, Amazônia Ocidental: Relato de caso. Arq. Bras. Med. Veterinária E Zootec. 2016, 68, 953–957. [Google Scholar] [CrossRef] [Green Version]
  31. Leschnik, M.; Kirtz, G.; Virányi, Z.; Wille-Piazzai, W.; Duscher, G. Acute Granulocytic Anaplasmosis in A Captive Timber Wolf (Canis Lupus Occidentalis). J. Zoo Wildl. Med. 2012, 43, 645–648. [Google Scholar] [CrossRef]
  32. Novacco, M.; Hofmann-Lehmann, R.; Grimm, F.; Meli, M.L.; Stirn, M. Fatal Acute Babesiosis Associated with Babesia Venatorum Infection (Babesia Sp. EU1) in a Captive Reindeer Calf in Switzerland. Vet. Parasitol. Reg. Stud. Rep. 2019, 18, 100336. [Google Scholar] [CrossRef]
  33. Romano, J.S.; Grund, L.; Obiegala, A.; Nymo, I.H.; Ancin-Murguzur, F.J.; Li, H.; Krol, N.; Pfeffer, M.; Tryland, M. A Multi-Pathogen Screening of Captive Reindeer (Rangifer tarandus) in Germany Based on Serological and Molecular Assays. Front. Vet. Sci. 2019, 6, 461. [Google Scholar] [CrossRef]
  34. Wiegmann, L.; Silaghi, C.; Obiegala, A.; Karnath, C.; Langer, S.; Ternes, K.; Kämmerling, J.; Osmann, C.; Pfeffer, M. Occurrence of Babesia Species in Captive Reindeer (Rangifer tarandus) in Germany. Vet. Parasitol. 2015, 211, 16–22. [Google Scholar] [CrossRef] [PubMed]
  35. Braks, M.A.H.; van Wieren, S.E.; Takken, W.; Sprong, H. Ecology and Prevention of Lyme Borreliosis; Wageningen Academic Publishers: Wageningen, The Netherlands, 2016; pp. 31–35. [Google Scholar]
  36. Larson, S.R.; Lee, X.; Paskewitz, S.M. Prevalence of Tick-Borne Pathogens in Two Species of Peromyscus Mice Common in Northern Wisconsin. J. Med. Entomol. 2018, 55, 1002–1010. [Google Scholar] [CrossRef]
  37. Cull, B.; Vaux, A.G.C.; Ottowell, L.J.; Gillingham, E.L.; Medlock, J.M. Tick Infestation of Small Mammals in an English Woodland. J. Vector Ecol. 2017, 42, 74–83. [Google Scholar] [CrossRef] [Green Version]
  38. Mendoza-Roldan, J.; Ribeiro, S.R.; Castilho-Onofrio, V.; Grazziotin, F.G.; Rocha, B.; Ferreto-Fiorillo, B.; Pereira, J.S.; Benelli, G.; Otranto, D.; Barros-Battesti, D.M. Mites and Ticks of Reptiles and Amphibians in Brazil. Acta Trop. 2020, 208, 105515. [Google Scholar] [CrossRef]
  39. Wilhelmsson, P.; Jaenson, T.G.T.; Olsen, B.; Waldenström, J.; Lindgren, P.-E. Migratory Birds as Disseminators of Ticks and the Tick-Borne Pathogens Borrelia Bacteria and Tick-Borne Encephalitis (TBE) Virus: A Seasonal Study at Ottenby Bird Observatory in South-Eastern Sweden. Parasit. Vectors 2020, 13, 607. [Google Scholar] [CrossRef]
  40. Hamer, S.A.; Goldberg, T.L.; Kitron, U.D.; Brawn, J.D.; Anderson, T.K.; Loss, S.R.; Walker, E.D.; Hamer, G.L. Wild Birds and Urban Ecology of Ticks and Tick-Borne Pathogens, Chicago, Illinois, USA, 2005–2010. Emerg. Infect. Dis. 2012, 18, 1589–1595. [Google Scholar] [CrossRef] [PubMed]
  41. Dimanopoulou, A.P.; Starras, A.G.; Diakou, A.; Lefkaditis, M.; Giadinis, N.D. Prevalence of Tick Species in Sheep and Goat Flocks in Areas of Southern Greece. J. Hell. Vet. Med. Soc. 2018, 68, 205. [Google Scholar] [CrossRef] [Green Version]
  42. Mysterud, A.; Hatlegjerde, I.L.; Sorensen, O.J. Attachment Site Selection of Life Stages of Ixodes Ricinus Ticks on a Main Large Host in Europe, the Red Deer (Cervus elaphus). Parasit. Vectors 2014, 7, 510. [Google Scholar] [CrossRef] [Green Version]
  43. Voordouw, M.J. Co-Feeding Transmission in Lyme Disease Pathogens. Parasitology 2015, 142, 290–302. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  44. Ferreri, L.; Bajardi, P.; Giacobini, M. Non-Systemic Transmission of Tick-Borne Diseases: A Network Approach. Commun. Nonlinear Sci. Numer. Simul. 2016, 39, 149–155. [Google Scholar] [CrossRef] [Green Version]
  45. Balashov, Y.S. Significance of Ixodid Tick (Parasitiformes, Ixodidae) Population Structure for Maintenance of Natural Foci of Infection. Biol. Bull. 2010, 37, 677–683. [Google Scholar] [CrossRef]
  46. Jaenson, T.G.T.; Petersson, E.H.; Jaenson, D.G.E.; Kindberg, J.; Pettersson, J.H.-O.; Hjertqvist, M.; Medlock, J.M.; Bengtsson, H. The Importance of Wildlife in the Ecology and Epidemiology of the TBE Virus in Sweden: Incidence of Human TBE Correlates with Abundance of Deer and Hares. Parasit. Vectors 2018, 11, 477. [Google Scholar] [CrossRef] [PubMed]
  47. Dzięgiel, B.; Adaszek, Ł.; Kalinowski, M.; Winiarczyk, S. Equine Granulocytic Anaplasmosis. Res. Vet. Sci. 2013, 95, 316–320. [Google Scholar] [CrossRef]
  48. Bournez, L.; Umhang, G.; Moinet, M.; Boucher, J.-M.; Demerson, J.-M.; Caillot, C.; Legras, L.; Devillers, E.; Hansmann, Y.; Velay, A.; et al. Disappearance of TBEV Circulation among Rodents in a Natural Focus in Alsace, Eastern France. Pathogens 2020, 9, 930. [Google Scholar] [CrossRef] [PubMed]
  49. Stanek, G. Pandora’s Box: Pathogens in Ixodes ricinus ticks in Central Europe. Wien. Klin. Wochenschr. 2009, 121, 673–683. [Google Scholar] [CrossRef]
  50. Eisen, L. Vector Competence Studies with Hard Ticks and Borrelia Burgdorferi Sensu Lato Spirochetes: A Review. Ticks Tick-Borne Dis. 2020, 11, 101359. [Google Scholar] [CrossRef]
  51. Václavík, T.; Balážová, A.; Baláž, V.; Tkadlec, E.; Schichor, M.; Zechmeisterová, K.; Ondruš, J.; Široký, P. Landscape Epidemiology of Neglected Tick-Borne Pathogens in Central Europe. Transbound. Emerg. Dis. 2020, 1–12. [Google Scholar] [CrossRef]
  52. Nelder, M.P.; Russell, C.B.; Sheehan, N.J.; Sander, B.; Moore, S.; Li, Y.; Johnson, S.; Patel, S.N.; Sider, D. Human Pathogens Associated with the Blacklegged Tick Ixodes Scapularis: A Systematic Review. Parasit. Vectors 2016, 9, 265. [Google Scholar] [CrossRef] [Green Version]
  53. Zieman, E.A.; Lawson, T.; Nielsen, C.K.; Jiménez, F.A. Within-Season Changes in Cytauxzoon Felis Parasitemia in Bobcats. J. Parasitol. 2020, 106, 308–311. [Google Scholar] [CrossRef]
  54. Guillemi, E.C.; Orozco, M.M.; Argibay, H.D.; Farber, M.D. Evidence of Ehrlichia Chaffeensis in Argentina through Molecular Detection in Marsh Deer (Blastocerus dichotomus). Int. J. Parasitol. Parasites Wildl. 2019, 8, 45–49. [Google Scholar] [CrossRef] [PubMed]
  55. Allan, B.F.; Goessling, L.S.; Storch, G.A.; Thach, R.E. Blood Meal Analysis to Identify Reservoir Hosts for Amblyomma Americanum Ticks. Emerg. Infect. Dis. 2010, 16, 433–440. [Google Scholar] [CrossRef]
  56. Mixson, T.R.; Campbell, S.R.; Gill, J.S.; Ginsberg, H.S.; Reichard, M.V.; Schulze, T.L.; Dasch, G.A. Prevalence of Ehrlichia, Borrelia, and Rickettsial Agents in Amblyomma Americanum (Acari: Ixodidae) Collected from Nine States. J. Med. Entomol. 2006, 43, 1261–1268. [Google Scholar] [CrossRef]
  57. Fritzen, C.M.; Huang, J.; Westby, K.; Freye, J.D.; Dunlap, B.; Yabsley, M.J.; Schardein, M.; Dunn, J.R.; Jones, T.F.; Moncayo, A.C. Infection Prevalences of Common Tick-Borne Pathogens in Adult Lone Star Ticks (Amblyomma americanum) and American Dog Ticks (Dermacentor variabilis) in Kentucky. Am. J. Trop. Med. Hyg. 2011, 85, 718–723. [Google Scholar] [CrossRef]
  58. Latrofa, M.S.; Dantas-Torres, F.; Giannelli, A.; Otranto, D. Molecular Detection of Tick-Borne Pathogens in Rhipicephalus Sanguineus Group Ticks. Ticks Tick-Borne Dis. 2014, 5, 943–946. [Google Scholar] [CrossRef]
  59. Dantas-Torres, F.; Otranto, D. Further Thoughts on the Taxonomy and Vector Role of Rhipicephalus Sanguineus Group Ticks. Vet. Parasitol. 2015, 208, 9–13. [Google Scholar] [CrossRef] [PubMed]
  60. Soares, R.L.; da Silva, A.O.; Coelho, M.L.; Echeverria, J.T.; de Souza, M.L.; Babo-Terra, V.J.; Pasquatti, T.N.; Ramos, R.A.N.; Ramos, C.A.D.N.; Soares, R.L.; et al. Molecular Detection of Cercopithifilaria Bainae and Other Tick-Borne Pathogens in Rhipicephalus Sanguineus s.l. Isolated from Dogs in Midwest Brazil. Rev. Bras. Parasitol. Veterinária 2020, 29. [Google Scholar] [CrossRef] [PubMed]
  61. Ogrzewalska, M.; Uezu, A.; Labruna, M.B. Ticks (Acari: Ixodidae) Infesting Wild Birds in the Eastern Amazon, Northern Brazil, with Notes on Rickettsial Infection in Ticks. Parasitol. Res. 2010, 106, 809–816. [Google Scholar] [CrossRef]
  62. Ogrzewalska, M.; Literak, I.; Cardenas-Callirgos, J.M.; Capek, M.; Labruna, M.B. Rickettsia Bellii in Ticks Amblyomma Varium Koch, 1844, from Birds in Peru. Ticks Tick-Borne Dis. 2012, 3, 254–256. [Google Scholar] [CrossRef]
  63. Lugarini, C.; Martins, T.F.; Ogrzewalska, M.; de Vasconcelos, N.C.T.; Ellis, V.A.; de Oliveira, J.B.; Pinter, A.; Labruna, M.B.; Silva, J.C.R. Rickettsial Agents in Avian Ixodid Ticks in Northeast Brazil. Ticks Tick-Borne Dis. 2015, 6, 364–375. [Google Scholar] [CrossRef]
  64. Labruna, M.B.; Whitworth, T.; Bouyer, D.H.; McBride, J.; Camargo, L.M.A.; Camargo, E.P.; Popov, V.; Walker, D.H. Rickettsia Bellii and Rickettsia Amblyommii in Amblyomma Ticks from the State of Rondônia, Western Amazon, Brazil. J. Med. Entomol. 2004, 41, 1073–1081. [Google Scholar] [CrossRef]
  65. Ogrzewalska, M.; Pacheco, R.C.; Uezu, A.; Richtzenhain, L.J.; Ferreira, F.; Labruna, M.B. Rickettsial Infection in Amblyomma Nodosum Ticks (Acari: Ixodidae) from Brazil. Ann. Trop. Med. Parasitol. 2009, 103, 413–425. [Google Scholar] [CrossRef]
  66. Miranda, J.; Portillo, A.; Oteo, J.A.; Mattar, S. Rickettsia Sp. Strain Colombianensi (Rickettsiales: Rickettsiaceae): A New Proposed Rickettsia Detected in Amblyomma Dissimile (Acari: Ixodidae) From Iguanas and Free-Living Larvae Ticks From Vegetation. J. Med. Entomol. 2012, 49, 960–965. [Google Scholar] [CrossRef]
  67. de Sousa, K.C.M.; Herrera, H.M.; Rocha, F.L.; Costa, F.B.; Martins, T.F.; Labruna, M.B.; Machado, R.Z.; André, M.R. Rickettsia Spp. among Wild Mammals and Their Respective Ectoparasites in Pantanal Wetland, Brazil. Ticks Tick-Borne Dis. 2018, 9, 10–17. [Google Scholar] [CrossRef] [Green Version]
  68. Luz, H.R.; Faccini, J.L.H.; McIntosh, D. Molecular Analyses Reveal an Abundant Diversity of Ticks and Rickettsial Agents Associated with Wild Birds in Two Regions of Primary Brazilian Atlantic Rainforest. Ticks Tick-Borne Dis. 2017, 8, 657–665. [Google Scholar] [CrossRef] [PubMed]
  69. Monje, L.D.; Nava, S.; Eberhardt, A.T.; Correa, A.I.; Guglielmone, A.A.; Beldomenico, P.M. Molecular Detection of the Human Pathogenic Rickettsia Sp. Strain Atlantic Rainforest in Amblyomma Dubitatum Ticks from Argentina. Vector-Borne Zoonotic Dis. 2015, 15, 167–169. [Google Scholar] [CrossRef]
  70. Harris, S.E.; Munshi-South, J. Signatures of Positive Selection and Local Adaptation to Urbanization in White-Footed Mice (Peromyscus leucopus). Mol. Ecol. 2017, 26, 6336–6350. [Google Scholar] [CrossRef] [PubMed]
  71. Michelitsch, A.; Wernike, K.; Klaus, C.; Dobler, G.; Beer, M. Exploring the Reservoir Hosts of Tick-Borne Encephalitis Virus. Viruses 2019, 11, 669. [Google Scholar] [CrossRef] [Green Version]
  72. Klaus, C.; Hoffmann, B.; Beer, M.; Müller, W.; Stark, B.; Bader, W.; Stiasny, K.; Heinz, F.X.; Süss, J. Seroprevalence of Tick-Borne Encephalitis (TBE) in Naturally Exposed Monkeys (Macaca sylvanus) and Sheep and Prevalence of TBE Virus in Ticks in a TBE Endemic Area in Germany. Ticks Tick-Borne Dis. 2010, 1, 141–144. [Google Scholar] [CrossRef] [PubMed]
  73. Krause, P.J.; Fish, D.; Narasimhan, S.; Barbour, A.G. Borrelia Miyamotoi Infection in Nature and in Humans. Clin. Microbiol. Infect. 2015, 21, 631–639. [Google Scholar] [CrossRef] [Green Version]
  74. Yoshii, K. Epidemiology and Pathological Mechanisms of Tick-Borne Encephalitis. J. Vet. Med. Sci. 2019, 81, 343–347. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  75. Paulsen, K.M.; Stuen, S.; das Neves, C.G.; Suhel, F.; Gurung, D.; Soleng, A.; Stiasny, K.; Vikse, R.; Andreassen, Å.K.; Granquist, E.G. Tick-Borne Encephalitis Virus in Cows and Unpasteurized Cow Milk from Norway. Zoonoses Public Health 2019, 66, 216–222. [Google Scholar] [CrossRef] [PubMed]
  76. Achazi, K.; Růžek, D.; Donoso-Mantke, O.; Schlegel, M.; Ali, H.S.; Wenk, M.; Schmidt-Chanasit, J.; Ohlmeyer, L.; Rühe, F.; Vor, T.; et al. Rodents as Sentinels for the Prevalence of Tick-Borne Encephalitis Virus. Vector Borne Zoonotic Dis. Larchmt. N 2011, 11, 641–647. [Google Scholar] [CrossRef] [Green Version]
  77. Duscher, G.G.; Leschnik, M.; Fuehrer, H.-P.; Joachim, A. Wildlife Reservoirs for Vector-Borne Canine, Feline and Zoonotic Infections in Austria. Int. J. Parasitol. Parasites Wildl. 2015, 4, 88–96. [Google Scholar] [CrossRef] [Green Version]
  78. Süss, J.; Gelpi, E.; Klaus, C.; Bagon, A.; Liebler-Tenorio, E.M.; Budka, H.; Stark, B.; Müller, W.; Hotzel, H. Tickborne Encephalitis in Naturally Exposed Monkey (Macaca sylvanus). Emerg. Infect. Dis. 2007, 13, 905–907. [Google Scholar] [CrossRef]
  79. Kenyon, R.H.; Rippy, M.K.; McKee, K.T.; Zack, P.M.; Peters, C.J. Infection of Macaca Radiata with Viruses of the Tick-Borne Encephalitis Group. Microb. Pathog. 1992, 13, 399–409. [Google Scholar] [CrossRef]
  80. Rumyantsev, A.A.; Chanock, R.M.; Murphy, B.R.; Pletnev, A.G. Comparison of Live and Inactivated Tick-Borne Encephalitis Virus Vaccines for Safety, Immunogenicity and Efficacy in Rhesus Monkeys. Vaccine 2006, 24, 133–143. [Google Scholar] [CrossRef]
  81. Cadavid, D. The Mammalian Host Response to Borrelia Infection. Wien. Klin. Wochenschr. 2006, 118, 653–658. [Google Scholar] [CrossRef]
  82. Gherman, C.M.; Sándor, A.D.; Kalmár, Z.; Marinov, M.; Mihalca, A.D. First Report of Borrelia Burgdorferi Sensu Lato in Two Threatened Carnivores: The Marbled Polecat, Vormela Peregusna and the European Mink, Mustela Lutreola (Mammalia: Mustelidae). BMC Vet. Res. 2012, 8, 137. [Google Scholar] [CrossRef] [Green Version]
  83. Honig, V.; Carolan, H.E.; Vavruskova, Z.; Massire, C.; Mosel, M.R.; Crowder, C.D.; Rounds, M.A.; Ecker, D.J.; Ruzek, D.; Grubhoffer, L.; et al. Broad-Range Survey of Vector-Borne Pathogens and Tick Host Identification of Ixodes Ricinus from Southern Czech Republic. FEMS Microbiol. Ecol. 2017, 93. [Google Scholar] [CrossRef] [PubMed]
  84. Grubhoffer, L.; Golovchenko, M.; Vancova, M.; Zacharovova-Slavickova, K.; Rudenko, N.; Oliver, J.H. Lyme Borreliosis: Insights into Tick- / Host-Borrelia Relations. Folia Parasitol. (Praha) 2005, 52, 279–294. [Google Scholar] [CrossRef] [Green Version]
  85. Petrulionienė, A.; Radzišauskienė, D.; Ambrozaitis, A.; Čaplinskas, S.; Paulauskas, A.; Venalis, A. Epidemiology of Lyme Disease in a Highly Endemic European Zone. Medicina (Mex.) 2020, 56, 115. [Google Scholar] [CrossRef] [Green Version]
  86. Nau, R.; Christen, H.-J.; Eiffert, H. Lyme Disease—Current State of Knowledge. Dtsch. Arztebl. Int. 2009, 106, 72–82. [Google Scholar] [CrossRef]
  87. Štefančíková, A.; Štěpánová, G.; Derdáková, M.; Pet’ko, B.; Kysel’ová, J.; Cigánek, J.; Strojný, L.; Čisláková, L.; Trávniček, M. Serological Evidence for Borrelia Burgdorferi Infection Associated with Clinical Signs in Dairy Cattle in Slovakia. Vet. Res. Commun. 2002, 26, 601–611. [Google Scholar] [CrossRef] [PubMed]
  88. Balmelli, T.; Piffaretti, J.-C. Association between Different Clinical Manifestations of Lyme Disease and Different Species of Borrelia Burgdorferi Sensu Lato. Res. Microbiol. 1995, 146, 329–340. [Google Scholar] [CrossRef]
  89. Coipan, E.C.; Jahfari, S.; Fonville, M.; Oei, G.A.; Spanjaard, L.; Takumi, K.; Hovius, J.W.R.; Sprong, H. Imbalanced Presence of Borrelia Burgdorferi s.l. Multilocus Sequence Types in Clinical Manifestations of Lyme Borreliosis. Infect. Genet. Evol. J. Mol. Epidemiol. Evol. Genet. Infect. Dis. 2016, 42, 66–76. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  90. Zhong, X.; Nouri, M.; Råberg, L. Colonization and Pathology of Borrelia Afzelii in Its Natural Hosts. Ticks Tick-Borne Dis. 2019, 10, 822–827. [Google Scholar] [CrossRef]
  91. Divers, T.J.; Gardner, R.B.; Madigan, J.E.; Witonsky, S.G.; Bertone, J.J.; Swinebroad, E.L.; Schutzer, S.E.; Johnson, A.L. Borrelia Burgdorferi Infection and Lyme Disease in North American Horses: A Consensus Statement. J. Vet. Intern. Med. 2018, 32, 617–632. [Google Scholar] [CrossRef] [Green Version]
  92. Bhide, M.; Yilmaz, Z.; Golcu, E.; Torun, S.; Mikula, I. Seroprevalence of Anti-Borrelia Burgdorferi Antibodies in Dogs and Horses in Turkey. Ann. Agric. Environ. Med. 2008, 15, 85–90. [Google Scholar]
  93. Appel, M.J.G.; Allan, S.; Jacobson, R.H.; Lauderdale, T.L.; Chang, Y.F.; Shin, S.J.; Thomford, J.W.; Todhunter, R.J.; Summers, B.A. Experimental Lyme Disease in Dogs Produces Arthritis and Persistent Infection. J. Infect. Dis. 1993, 167, 651–654. [Google Scholar] [CrossRef]
  94. Borys, M.A.; Kass, P.H.; Mohr, F.C.; Sykes, J.E. Differences in Clinicopathologic Variables between Borrelia C6 Antigen Seroreactive and Borrelia C6 Seronegative Glomerulopathy in Dogs. J. Vet. Intern. Med. 2019, 33, 2096–2104. [Google Scholar] [CrossRef] [Green Version]
  95. Belperron, A.A.; Bockenstedt, L.K. Natural Antibody Affects Survival of the Spirochete Borrelia Burgdorferi within Feeding Ticks. Infect. Immun. 2001, 69, 6456–6462. [Google Scholar] [CrossRef] [Green Version]
  96. Bhide, M.R.; Travnicek, M.; Levkutova, M.; Curlik, J.; Revajova, V.; Levkut, M. Sensitivity of Borrelia Genospecies to Serum Complement from Different Animals and Human: A Host–Pathogen Relationship. FEMS Immunol. Med. Microbiol. 2005, 43, 165–172. [Google Scholar] [CrossRef] [Green Version]
  97. Bos, J.H.; Klip, F.C.; Sprong, H.; Broens, E.M.; Kik, M.J.L. Clinical Outbreak of Babesiosis Caused by Babesia Capreoli in Captive Reindeer (Rangifer tarandus Tarandus) in the Netherlands. Ticks Tick-Borne Dis. 2017, 8, 799–801. [Google Scholar] [CrossRef] [PubMed]
  98. Milnes, E.L.; Thornton, G.L.; Delnatte, P.; Léveillé, A.N.; Barta, J.R.; Smith, D.A.; Nemeth, N.M. Molecular Detection of Babesia Odocoilei in Wild, Farmed, and Zoo Cervids in Ontario, Canada. J. Wildl. Dis. 2019, 55, 335–342. [Google Scholar] [CrossRef]
  99. Schoelkopf, L.; Hutchinson, C.E.; Bendele, K.G.; Goff, W.L.; Willette, M.; Rasmussen, J.M.; Holman, P.J. New Ruminant Hosts and Wider Geographic Range Identified For Babesia Odocoilei (Emerson and Wright 1970). J. Wildl. Dis. 2005, 41, 683–690. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  100. Hildebrandt, A.; Gray, J.S.; Hunfeld, K.-P. Human Babesiosis in Europe: What Clinicians Need to Know. Infection 2013, 41, 1057–1072. [Google Scholar] [CrossRef]
  101. Holman, P.J.; Craig, T.M.; Crider, D.L.D.; Petrini, K.R.; Rhyan, J.; Wagner, G.G. Culture Isolation and Partial Characterization of a Babesia Sp. from a North American Elk (Cervus elaphus). J. Wildl. Dis. 1994, 30, 460–465. [Google Scholar] [CrossRef] [PubMed]
  102. Schnittger, L.; Rodriguez, A.E.; Florin-Christensen, M.; Morrison, D.A. Babesia: A World Emerging. Infect. Genet. Evol. 2012, 12, 1788–1809. [Google Scholar] [CrossRef] [PubMed]
  103. Kik, M.; Nijhof, A.M.; Balk, J.A.; Jongejan, F. Babesia Sp. EU1 Infection in a Forest Reindeer, the Netherlands. Emerg. Infect. Dis. 2011, 17, 936–938. [Google Scholar] [CrossRef] [PubMed]
  104. Langton, C.; Gray, J.; Waters, P.; Holman, P. Naturally Acquired Babesiosis in a Reindeer (Rangifer tarandus Tarandus) Herd in Great Britain. Parasitol. Res. 2003, 89, 194–198. [Google Scholar] [CrossRef] [PubMed]
  105. Pattullo, K.M.; Wobeser, G.; Lockerbie, B.P.; Burgess, H.J. Babesia Odocoilei Infection in a Saskatchewan Elk (Cervus elaphus canadensis) Herd. J. Vet. Diagn. Invest. 2013, 25, 535–540. [Google Scholar] [CrossRef] [PubMed]
  106. Petrini, K.R.; Holman, P.J.; Rhyan, J.C.; Jenkins, S.J.; Wagner, G.G. Fatal Babesiosis in an American Woodland Caribou (Rangifer tarandus caribou). J. Zoo Wildl. Med. 1995, 26, 298–305. [Google Scholar]
  107. Gallatin, L.L.; Irizarry-Rovira, A.R.; Renninger, M.L.; Holman, P.J.; Wagner, G.G.; Sojka, J.E.; Christian, J.A. Babesia Odocoilei Infection in Elk. J. Am. Vet. Med. Assoc. 2003, 223, 1027–1032. [Google Scholar] [CrossRef]
  108. Bartlett, S.L.; Abou-Madi, N.; Messick, J.B.; Birkenheuer, A.; Kollias, G.V. Diagnosis and Treatment of Babesia Odocoilei in Captive Reindeer (Rangifer tarandus Tarandus) and Recognition of Three Novel Host Species. J. Zoo Wildl. Med. 2009, 40, 152–159. [Google Scholar] [CrossRef]
  109. André, M.R.; Adania, C.H.; Teixeira, R.H.F.; Allegretti, S.M.; Machado, R.Z. Molecular and Serological Detection of Babesia Spp. in Neotropical and Exotic Carnivores in Brazilian Zoos. J. Zoo Wildl. Med. 2011, 42, 139–143. [Google Scholar] [CrossRef]
  110. André, M.R.; Baccarim Denardi, N.C.; Marques de Sousa, K.C.; Gonçalves, L.R.; Henrique, P.C.; Grosse Rossi Ontivero, C.R.; Lima Gonzalez, I.H.; Cabral Nery, C.V.; Fernandes Chagas, C.R.; Monticelli, C.; et al. Arthropod-Borne Pathogens Circulating in Free-Roaming Domestic Cats in a Zoo Environment in Brazil. Ticks Tick-Borne Dis. 2014, 5, 545–551. [Google Scholar] [CrossRef]
  111. Phair, K.A.; Carpenter, J.W.; Smee, N.; Myers, C.B.; Pohlman, L.M. Severe Anemia Caused by Babesiosis in a Maned Wolf (Chrysocyon brachyurus). J. Zoo Wildl. Med. 2012, 43, 162–167. [Google Scholar] [CrossRef] [Green Version]
  112. Wasserkrug Naor, A.; Lindemann, D.M.; Schreeg, M.E.; Marr, H.S.; Birkenheuer, A.J.; Carpenter, J.W.; Ryseff, J.K. Clinical, Morphological, and Molecular Characterization of an Undetermined Babesia Species in a Maned Wolf (Chrysocyon brachyurus). Ticks Tick-Borne Dis. 2019, 10, 124–126. [Google Scholar] [CrossRef]
  113. Mans, B.J.; Pienaar, R.; Latif, A.A. A Review of Theileria Diagnostics and Epidemiology. Int. J. Parasitol. Parasites Wildl. 2015, 4, 104–118. [Google Scholar] [CrossRef] [Green Version]
  114. André, M.R.; Adania, C.H.; Machado, R.Z.; Allegretti, S.M.; Felippe, P.A.N.; Silva, K.F.; Nakaghi, A.C.H.; Dagnone, A.S. Molecular Detection of Cytauxzoon Spp. in Asymptomatic Brazilian Wild Captive Felids. J. Wildl. Dis. 2009, 45, 234–237. [Google Scholar] [CrossRef] [Green Version]
  115. Peixoto, P.V.; Soares, C.O.; Scofield, A.; Santiago, C.D.; França, T.N.; Barros, S.S. Fatal Cytauxzoonosis in Captive-Reared Lions in Brazil. Vet. Parasitol. 2007, 145, 383–387. [Google Scholar] [CrossRef]
  116. Sivakumar, T.; Hayashida, K.; Sugimoto, C.; Yokoyama, N. Evolution and Genetic Diversity of Theileria. Infect. Genet. Evol. 2014, 27, 250–263. [Google Scholar] [CrossRef] [Green Version]
  117. Yam, J.; Gestier, S.; Bryant, B.; Campbell-Ward, M.; Bogema, D.; Jenkins, C. The Identification of Theileria Bicornis in Captive Rhinoceros in Australia. Int. J. Parasitol. Parasites Wildl. 2018, 7, 85–89. [Google Scholar] [CrossRef] [PubMed]
  118. Osman, S.A.; Al-Gaabary, M.H. Clinical, Haematological and Therapeutic Studies on Tropical Theileriosis in Water Buffaloes (Bubalus Bubalis) in Egypt. Vet. Parasitol. 2007, 146, 337–340. [Google Scholar] [CrossRef] [PubMed]
  119. Oakes, V.J.; Yabsley, M.J.; Schwartz, D.; LeRoith, T.; Bissett, C.; Broaddus, C.; Schlater, J.L.; Todd, S.M.; Boes, K.M.; Brookhart, M.; et al. Theileria Orientalis Ikeda Genotype in Cattle, Virginia, USA. Emerg. Infect. Dis. 2019, 25, 1653–1659. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  120. Garner, B.C.; Holman, P.; Berent, L.M. Theileriosis in a Reindeer (Rangifer tarandus Tarandus) Associated with a Potentially Novel Theileria Sp. Vet. Clin. Pathol. 2012, 41, 497–501. [Google Scholar] [CrossRef]
  121. de Souza Gonçalves, T.; de Nazaré Leite Barros, F.; Inoue, L.S.; de Farias, D.M.; dos Santos Lima, J.; Nobre, A.V.; Azenha Aidar, E.S.; Ferreira Diniz, R.R.; Gering, A.P.; Scofield, A. Natural Theileria Equi Infection in Captive Tapirus Terrestris (Perissodactyla: Tapiridae) in the Brazilian Amazon. Ticks Tick-Borne Dis. 2020, 11, 101452. [Google Scholar] [CrossRef]
  122. Filoni, C.; Catão-Dias, J.L.; Cattori, V.; Willi, B.; Meli, M.L.; Corrêa, S.H.R.; Marques, M.C.; Adania, C.H.; Silva, J.C.R.; Marvulo, M.F.V.; et al. Surveillance Using Serological and Molecular Methods for the Detection of Infectious Agents in Captive Brazilian Neotropic and Exotic Felids. J. Vet. Diagn. Invest. 2011. [Google Scholar] [CrossRef] [Green Version]
  123. Garner, M.M.; Lung, N.P.; Citino, S.; Greiner, E.C.; Harvey, J.W.; Homer, B.L. Fatal Cytauxzoonosis in a Captive-Reared White Tiger (Panthera Tigris). Vet. Pathol. 1996, 33, 82–86. [Google Scholar] [CrossRef]
  124. Clarke, L.L.; Rissi, D.R. Neuropathology of Natural Cytauxzoon Felis Infection in Domestic Cats. Vet. Pathol. 2015, 52, 1167–1171. [Google Scholar] [CrossRef] [Green Version]
  125. Aschenbroich, S.A.; Rech, R.R.; Sousa, R.S.; Carmichael, K.P.; Sakamoto, K. Pathology in Practice. Cytauxzoon Felis Infection. J. Am. Vet. Med. Assoc. 2012, 240, 159–161. [Google Scholar] [CrossRef]
  126. Lu, M.; Li, F.; Liao, Y.; Shen, J.-J.; Xu, J.-M.; Chen, Y.-Z.; Li, J.-H.; Holmes, E.C.; Zhang, Y.-Z. Epidemiology and Diversity of Rickettsiales Bacteria in Humans and Animals in Jiangsu and Jiangxi Provinces, China. Sci. Rep. 2019, 9, 13176. [Google Scholar] [CrossRef]
  127. Yabsley, M.J.; Norton, T.M.; Powell, M.R.; Davidson, W.R. Molecular and Serologic Evidence of Tick-Borne Ehrlichiae in Three Species of Lemurs from St. Catherines Island, Georgia, USA. J. Zoo Wildl. Med. 2004, 35, 503–509. [Google Scholar] [CrossRef]
  128. Yu, X.-J.; Walker, D.H. The Order Rickettsiales. In The Prokaryotes; Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K.-H., Stackebrandt, E., Eds.; Springer New York: New York, NY, USA, 2006; pp. 493–528. [Google Scholar]
  129. Seo, M.-G.; Kwon, O.-D.; Kwak, D. Anaplasma Bovis Infection in a Horse: First Clinical Report and Molecular Analysis. Vet. Microbiol. 2019, 233, 47–51. [Google Scholar] [CrossRef]
  130. Torina, A.; Naranjo, V.; Pennisi, M.G.; Patania, T.; Vitale, F.; Laricchiuta, P.; Alongi, A.; Scimeca, S.; Kocan, K.M.; Fuente, J. De La Serologic And Molecular Characterization of Tick-Borne Pathogens In Lions (Panthera leo) from the Fasano Safari Park, Italy. J. Zoo Wildl. Med. 2007, 38, 591–593. [Google Scholar] [CrossRef] [PubMed]
  131. André, M.R.; Adania, C.H.; Machado, R.Z.; Allegretti, S.M.; Felippe, P.A.N.; Silva, K.F.; Nakaghi, A.C.H. Molecular and Serologic Detection of Ehrlichia Spp. in Endangered Brazilian Wild Captive Felids. J. Wildl. Dis. 2010, 46, 1017–1023. [Google Scholar] [CrossRef] [PubMed]
  132. André, M.R.; Dumler, J.S.; Scorpio, D.G.; Teixeira, R.H.F.; Allegretti, S.M.; Machado, R.Z. Molecular Detection of Tick-Borne Bacterial Agents in Brazilian and Exotic Captive Carnivores. Ticks Tick-Borne Dis. 2012, 3, 247–253. [Google Scholar] [CrossRef]
  133. Zhang, Y.; Li, T.; Cui, Y.; Wang, J.; Lv, Y.; Wang, R.; Jian, F.; Zhang, L.; Wang, J.; Yang, G.; et al. The First Report of Anaplasma Phagocytophilum and a Novel Theileria Spp. Co-Infection in a South African Giraffe. Parasitol. Int. 2016, 65, 347–351. [Google Scholar] [CrossRef] [PubMed]
  134. Matsuno, K.; Nonoue, N.; Noda, A.; Kasajima, N.; Noguchi, K.; Takano, A.; Shimoda, H.; Orba, Y.; Muramatsu, M.; Sakoda, Y.; et al. Fatal Tickborne Phlebovirus Infection in Captive Cheetahs, Japan. Emerg. Infect. Dis. 2018, 24, 1726–1729. [Google Scholar] [CrossRef]
  135. Benelli, G. Pathogens Manipulating Tick Behavior—Through a Glass, Darkly. Pathogens 2020, 9, 664. [Google Scholar] [CrossRef] [PubMed]
  136. Inci, A.; Yildirim, A.; Duzlu, O.; Doganay, M.; Aksoy, S. Tick-Borne Diseases in Turkey: A Review Based on One Health Perspective. PLoS Negl. Trop. Dis. 2016, 10, e0005021. [Google Scholar] [CrossRef]
  137. Otranto, D.; Brianti, E.; Dantas-Torres, F.; Miró, G.; Latrofa, M.S.; Mutafchiev, Y.; Bain, O. Species Diversity of Dermal Microfilariae of the Genus Cercopithifilaria Infesting Dogs in the Mediterranean Region. Parasitology 2013, 140, 99–108. [Google Scholar] [CrossRef] [PubMed]
  138. Otranto, D.; Varcasia, A.; Solinas, C.; Scala, A.; Brianti, E.; Dantas-Torres, F.; Annoscia, G.; Martin, C.; Mutafchiev, Y.; Bain, O. Redescription of Cercopithifilaria Bainae Almeida & Vicente, 1984 (Spirurida, Onchocercidae) from a Dog in Sardinia, Italy. Parasit. Vectors 2013, 6, 132. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  139. Tahir, D.; Davoust, B.; Parola, P. Vector-Borne Nematode Diseases in Pets and Humans in the Mediterranean Basin: An Update. Vet. World 2019, 12, 1630–1643. [Google Scholar] [CrossRef] [Green Version]
  140. Szatmari, V.; van Leeuwen, M.W.; Piek, C.J.; Venco, L. False Positive Antigen Test for Dirofilaria Immitis after Heat Treatment of the Blood Sample in a Microfilaremic Dog Infected with Acanthocheilonema Dracunculoides. Parasit. Vectors 2020, 13, 501. [Google Scholar] [CrossRef] [PubMed]
  141. Uni, S.; Bain, O.; Fujita, H.; Matsubayashi, M.; Fukuda, M.; Takaoka, H. Infective Larvae of Cercopithifilaria Spp. (Nematoda: Onchocercidae) from Hard Ticks (Ixodidae) Recovered from the Japanese Serow (Bovidae). Parasite 2013, 20, 1. [Google Scholar] [CrossRef] [Green Version]
  142. Zhang, X.; Norris, D.E.; Rasgon, J.L. Distribution and Molecular Characterization of Wolbachia Endosymbionts and Filarial Nematodes in Maryland Populations of the Lone Star Tick (Amblyomma americanum). FEMS Microbiol. Ecol. 2011, 77, 50–56. [Google Scholar] [CrossRef]
  143. Tokarz, R.; Tagliafierro, T.; Sameroff, S.; Cucura, D.M.; Oleynik, A.; Che, X.; Jain, K.; Lipkin, W.I. Microbiome Analysis of Ixodes Scapularis Ticks from New York and Connecticut. Ticks Tick-Borne Dis. 2019, 10, 894–900. [Google Scholar] [CrossRef]
  144. Namrata, P.; Miller, J.M.; Shilpa, M.; Reddy, P.R.; Bandoski, C.; Rossi, M.J.; Sapi, E. Filarial Nematode Infection in Ixodes Scapularis Ticks Collected from Southern Connecticut. Vet. Sci. 2014, 1, 5–15. [Google Scholar] [CrossRef]
  145. Olmeda-García, A.S.; Rodríguez-Rodríguez, J.A. Stage-Specific Development of a Filarial Nematode (Dipetalonema dracunculoides) in Vector Ticks. J. Helminthol. 1994, 68, 231–235. [Google Scholar] [CrossRef] [PubMed]
  146. Brianti, E.; Otranto, D.; Dantas-Torres, F.; Weigl, S.; Latrofa, M.S.; Gaglio, G.; Napoli, E.; Brucato, G.; Cauquil, L.; Giannetto, S.; et al. Rhipicephalus Sanguineus (Ixodida, Ixodidae) as Intermediate Host of a Canine Neglected Filarial Species with Dermal Microfilariae. Vet. Parasitol. 2012, 183, 330–337. [Google Scholar] [CrossRef] [PubMed]
  147. Parker, J.; White, K. Lyme Borreliosis in Cattle and Horses-a Review of the Literature. Cornell Vet. 1992, 82, 253–274. [Google Scholar] [PubMed]
  148. Gusset, M.; Dick, G. The Global Reach of Zoos and Aquariums in Visitor Numbers and Conservation Expenditures. Zoo Biol. 2011, 30, 566–569. [Google Scholar] [CrossRef] [PubMed]
  149. Little, S.E.; Barrett, A.W.; Nagamori, Y.; Herrin, B.H.; Normile, D.; Heaney, K.; Armstrong, R. Ticks from Cats in the United States: Patterns of Infestation and Infection with Pathogens. Vet. Parasitol. 2018, 257, 15–20. [Google Scholar] [CrossRef]
  150. Panait, L.C.; Stock, G.; Globokar, M.; Balzer, J.; Groth, B.; Mihalca, A.D.; Pantchev, N. First Report of Cytauxzoon Sp. Infection in Germany: Organism Description and Molecular Confirmation in a Domestic Cat. Parasitol. Res. 2020, 119, 3005–3011. [Google Scholar] [CrossRef] [PubMed]
  151. Penzhorn, B.L.; Oosthuizen, M.C. Babesia Species of Domestic Cats: Molecular Characterization Has Opened Pandora’s Box. Front. Vet. Sci. 2020, 7, 134. [Google Scholar] [CrossRef]
  152. Ma, J.; Hine, P.M.; Clough, E.R.; Fish, D.; Coughlin, R.T.; Beltz, G.A.; Shew, M.G. Safety, Efficacy, and Immunogenicity of a Recombinant Osp Subunit Canine Lyme Disease Vaccine. Vaccine 1996, 14, 1366–1374. [Google Scholar] [CrossRef]
  153. Guarino, C.; Asbie, S.; Rohde, J.; Glaser, A.; Wagner, B. Vaccination of Horses with Lyme Vaccines for Dogs Induces Short-Lasting Antibody Responses. Vaccine 2017, 35, 4140–4147. [Google Scholar] [CrossRef]
  154. Torina, A.; Moreno-Cid, J.A.; Blanda, V.; Fernández de Mera, I.G.; de la Lastra, J.M.P.; Scimeca, S.; Blanda, M.; Scariano, M.E.; Briganò, S.; Disclafani, R.; et al. Control of Tick Infestations and Pathogen Prevalence in Cattle and Sheep Farms Vaccinated with the Recombinant Subolesin-Major Surface Protein 1a Chimeric Antigen. Parasit. Vectors 2014, 7, 10. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  155. Černý, J.; Lynn, G.; Hrnková, J.; Golovchenko, M.; Rudenko, N.; Grubhoffer, L. Management Options for Ixodes Ricinus-Associated Pathogens: A Review of Prevention Strategies. Int. J. Environ. Res. Public. Health 2020, 17, 1830. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  156. Hokynar, K.; Sormunen, J.J.; Vesterinen, E.J.; Partio, E.K.; Lilley, T.; Timonen, V.; Panelius, J.; Ranki, A.; Puolakkainen, M. Chlamydia-Like Organisms (CLOs) in Finnish Ixodes Ricinus Ticks and Human Skin. Microorganisms 2016, 4, 28. [Google Scholar] [CrossRef] [Green Version]
  157. Croxatto, A.; Rieille, N.; Kernif, T.; Bitam, I.; Aeby, S.; Péter, O.; Greub, G. Presence of Chlamydiales DNA in Ticks and Fleas Suggests That Ticks Are Carriers of Chlamydiae. Ticks Tick-Borne Dis. 2014, 5, 359–365. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  158. Pilloux, L.; Aeby, S.; Gaümann, R.; Burri, C.; Beuret, C.; Greub, G. The High Prevalence and Diversity of Chlamydiales DNA within Ixodes Ricinus Ticks Suggest a Role for Ticks as Reservoirs and Vectors of Chlamydia-Related Bacteria. Appl. Environ. Microbiol. 2015, 81, 8177–8182. [Google Scholar] [CrossRef] [Green Version]
  159. Burnard, D.; Weaver, H.; Gillett, A.; Loader, J.; Flanagan, C.; Polkinghorne, A. Novel Chlamydiales Genotypes Identified in Ticks from Australian Wildlife. Parasit. Vectors 2017, 10, 46. [Google Scholar] [CrossRef] [Green Version]
  160. Cheong, H.C.; Lee, C.Y.Q.; Cheok, Y.Y.; Tan, G.M.Y.; Looi, C.Y.; Wong, W.F. Chlamydiaceae: Diseases in Primary Hosts and Zoonosis. Microorganisms 2019, 7, 146. [Google Scholar] [CrossRef] [Green Version]
  161. Fritschi, J.; Marti, H.; Seth-Smith, H.M.B.; Aeby, S.; Greub, G.; Meli, M.L.; Hofmann-Lehmann, R.; Mühldorfer, K.; Stokar-Regenscheit, N.; Wiederkehr, D.; et al. Prevalence and Phylogeny of Chlamydiae and Hemotropic Mycoplasma Species in Captive and Free-Living Bats. BMC Microbiol. 2020, 20, 182. [Google Scholar] [CrossRef]
  162. Osman, K.M.; Ali, H.A.; ElJakee, J.A.; Galal, H.M. Prevalence of Chlamydophila Psittaci Infections in the Eyes of Cattle, Buffaloes, Sheep and Goats in Contact with a Human Population. Transbound. Emerg. Dis. 2013, 60, 245–251. [Google Scholar] [CrossRef]
  163. Greco, G.; Corrente, M.; Buonavoglia, D.; Campanile, G.; Di Palo, R.; Martella, V.; Bellacicco, A.L.; D’Abramo, M.; Buonavoglia, C. Epizootic Abortion Related to Infections by Chlamydophila Abortus and Chlamydophila Pecorum in Water Buffalo (Bubalus bubalis). Theriogenology 2008, 69, 1061–1069. [Google Scholar] [CrossRef]
  164. Wu, S.-M.; Huang, S.-Y.; Xu, M.-J.; Zhou, D.-H.; Song, H.-Q.; Zhu, X.-Q. Chlamydia Felis Exposure in Companion Dogs and Cats in Lanzhou, China: A Public Health Concern. BMC Vet. Res. 2013, 9, 104. [Google Scholar] [CrossRef] [Green Version]
  165. Schautteet, K.; Vanrompay, D. Chlamydiaceae Infections in Pig. Vet. Res. 2011, 42, 29. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  166. Petersen, J.M.; Mead, P.S.; Schriefer, M.E. Francisella Tularensis: An Arthropod-Borne Pathogen. Vet. Res. 2009, 40, 7. [Google Scholar] [CrossRef] [Green Version]
  167. Zellner, B.; Huntley, J.F. Ticks and Tularemia: Do We Know What We Don’t Know? Front. Cell. Infect. Microbiol. 2019, 9, 146. [Google Scholar] [CrossRef] [PubMed]
  168. Beckwith, C.S. Tularemia as a Cause of Fever in a Squirrel Monkey. J. Am. Vet. Med. Assoc. 2006, 229, 269–273. [Google Scholar] [CrossRef] [PubMed]
  169. Calle, P.P.; Bowerman, D.L.; Pape, W.J. Nonhuman Primate Tularemia (Francisella tularensis) Epizootic in a Zoological Park. J. Zoo Wildl. Med. 1993, 24, 459–468. [Google Scholar]
  170. Kuehn, A.; Schulze, C.; Kutzer, P.; Probst, C.; Hlinak, A.; Ochs, A.; Grunow, R. Tularaemia Seroprevalence of Captured and Wild Animals in Germany: The Fox (Vulpes vulpes) as a Biological Indicator. Epidemiol. Infect. 2013, 141, 833–840. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  171. Preiksaitis, J.K.; Crawshaw, G.J.; Nayar, G.S.; Stiver, H.G. Human Tularemia at an Urban Zoo. Can. Med. Assoc. J. 1979, 121, 1097–1099. [Google Scholar]
  172. Wechtaisong, W.; Bonnet, S.I.; Lien, Y.-Y.; Chuang, S.-T.; Tsai, Y.-L. Transmission of Bartonella Henselae within Rhipicephalus Sanguineus: Data on the Potential Vector Role of the Tick. PLoS Negl. Trop. Dis. 2020, 14, e0008664. [Google Scholar] [CrossRef]
  173. Asyikha, R.; Sulaiman, N.; Mohd-Taib, F.S. Detection of Bartonella Sp. in Ticks and Their Small Mammal Hosts in Mangrove Forests of Peninsular Malaysia. Trop. Biomed. 2020, 37, 919–931. [Google Scholar]
  174. Levytska, V.A.; Mushinsky, A.B.; Zubrikova, D.; Blanarova, L.; Dlugosz, E.; Vichova, B.; Slivinska, K.A.; Gajewski, Z.; Gizinski, S.; Liu, S.; et al. Detection of Pathogens in Ixodid Ticks Collected from Animals and Vegetation in Five Regions of Ukraine. Ticks Tick-Borne Dis. 2021, 12, 101586. [Google Scholar] [CrossRef] [PubMed]
  175. Ghafar, A.; Cabezas-Cruz, A.; Galon, C.; Obregon, D.; Gasser, R.B.; Moutailler, S.; Jabbar, A. Bovine Ticks Harbour a Diverse Array of Microorganisms in Pakistan. Parasit. Vectors 2020, 13, 1. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  176. Breitschwerdt, E.B.; Maggi, R.G.; Chomel, B.B.; Lappin, M.R. Bartonellosis: An Emerging Infectious Disease of Zoonotic Importance to Animals and Human Beings. J. Vet. Emerg. Crit. Care 2010, 20, 8–30. [Google Scholar] [CrossRef]
  177. Ebani, V.V.; Guardone, L.; Marra, F.; Altomonte, I.; Nardoni, S.; Mancianti, F. Arthropod-Borne Pathogens in Stray Cats from Northern Italy: A Serological and Molecular Survey. Animals 2020, 10, 2334. [Google Scholar] [CrossRef]
  178. Selmi, R.; Ben Said, M.; Ben Yahia, H.; Abdelaali, H.; Boulouis, H.-J.; Messadi, L. First Report on Bartonella Henselae in Dromedary Camels (Camelus dromedarius). Infect. Genet. Evol. 2020, 85, 104496. [Google Scholar] [CrossRef] [PubMed]
  179. Hao, L.; Yuan, D.; Guo, L.; Hou, W.; Mo, X.; Yin, J.; Yang, A.; Li, R. Molecular Detection of Bartonella in Ixodid Ticks Collected from Yaks and Plateau Pikas (Ochotona curzoniae) in Shiqu County, China. BMC Vet. Res. 2020, 16, 235. [Google Scholar] [CrossRef] [PubMed]
  180. Boularias, G.; Azzag, N.; Gandoin, C.; Bouillin, C.; Chomel, B.; Haddad, N.; Boulouis, H.J. Bartonella Bovis and Bartonella Chomelii Infection in Dairy Cattle and Their Ectoparasites in Algeria. Comp. Immunol. Microbiol. Infect. Dis. 2020, 70, 101450. [Google Scholar] [CrossRef] [PubMed]
  181. Chochlakis, D.; Cutler, S.; Giadini, N.D.; Psaroulaki, A. Bartonella Vinsonii Subsp. Arupensis Infection in Animals of Veterinary Importance, Ticks and Biopsy Samples. New Microbes New Infect. 2020, 34, 100652. [Google Scholar] [CrossRef]
  182. Grech-Angelini, S.; Stachurski, F.; Vayssier-Taussat, M.; Devillers, E.; Casabianca, F.; Lancelot, R.; Uilenberg, G.; Moutailler, S. Tick-Borne Pathogens in Ticks (Acari: Ixodidae) Collected from Various Domestic and Wild Hosts in Corsica (France), a Mediterranean Island Environment. Transbound. Emerg. Dis. 2020, 67, 745–757. [Google Scholar] [CrossRef]
  183. Ben-Harari, R.R. Tick Transmission of Toxoplasmosis. Expert Rev. Anti Infect. Ther. 2019, 17, 911–917. [Google Scholar] [CrossRef]
  184. Sroka, J.; Chmielewska-Badora, J.; Dutkiewicz, J. Ixodes Ricinus as a Potential Vector of Toxoplasma Gondii. Ann. Agric. Environ. Med. AAEM 2003, 10, 121–123. [Google Scholar] [PubMed]
Figure 1. Ticks and tick-borne pathogens reported from zoo-housed animals: Ticks (A) or tick-borne pathogens (B) feeding on/detected in zoo-housed animals were found in all countries where this kind of research was performed. It indicates that zoo-housed animals may serve as hosts and reservoirs for local/established but also imported ticks and tick-borne pathogens. Nevertheless, lack of wider data and their anecdotal nature does not allow us to make definitive presumptions. Further research is needed to help us in understanding of the role of zoo-housed animals in tick biology. TBEV—tick-borne encephalitis virus. SFTSV—severe fever and thrombocytopenia syndrome phlebovirus
Figure 1. Ticks and tick-borne pathogens reported from zoo-housed animals: Ticks (A) or tick-borne pathogens (B) feeding on/detected in zoo-housed animals were found in all countries where this kind of research was performed. It indicates that zoo-housed animals may serve as hosts and reservoirs for local/established but also imported ticks and tick-borne pathogens. Nevertheless, lack of wider data and their anecdotal nature does not allow us to make definitive presumptions. Further research is needed to help us in understanding of the role of zoo-housed animals in tick biology. TBEV—tick-borne encephalitis virus. SFTSV—severe fever and thrombocytopenia syndrome phlebovirus
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Figure 2. Differences in sampling for TBPs in zoo-housed animals (divided by orders). From this histogram, we can note the lack of testing in the Preissodactyla and Primates order. The orders Struthioniformes (2 samples), Phoenicopteriformes (1 sample), Testudines (1 sample), Squamata (1 sample) and Crocodilia (3 samples) have been tested only for Borrelia antibodies and in such small numbers that it would not provide any graphical value in the histogram. The role of these orders in the overall TBPs ecology is unclear; information is isolated only on the one tested pathogen. Some orders of animals, which are potentially threatened by TBPs and ticks, are omitted completely. For example: Chiroptera, Dermoptera, Edentata, Insectivora, Lagomorpha, Marsupialia, Proboscidea and Pholidata which all have the potential to carry ticks and therefore contract TBDs. Species from these orders are often kept in zoos in outdoor or semi-outdoor enclosures and the contact with ticks can occur. This suggests further need for the increase in research of the omitted or lacking animal orders.
Figure 2. Differences in sampling for TBPs in zoo-housed animals (divided by orders). From this histogram, we can note the lack of testing in the Preissodactyla and Primates order. The orders Struthioniformes (2 samples), Phoenicopteriformes (1 sample), Testudines (1 sample), Squamata (1 sample) and Crocodilia (3 samples) have been tested only for Borrelia antibodies and in such small numbers that it would not provide any graphical value in the histogram. The role of these orders in the overall TBPs ecology is unclear; information is isolated only on the one tested pathogen. Some orders of animals, which are potentially threatened by TBPs and ticks, are omitted completely. For example: Chiroptera, Dermoptera, Edentata, Insectivora, Lagomorpha, Marsupialia, Proboscidea and Pholidata which all have the potential to carry ticks and therefore contract TBDs. Species from these orders are often kept in zoos in outdoor or semi-outdoor enclosures and the contact with ticks can occur. This suggests further need for the increase in research of the omitted or lacking animal orders.
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Table 1. The prevalence of Borrelia specific antibodies in exotic zoo animals in Czech Republic and Germany together with observed borrelicidal effect of zoo animal sera.
Table 1. The prevalence of Borrelia specific antibodies in exotic zoo animals in Czech Republic and Germany together with observed borrelicidal effect of zoo animal sera.
GroupFamilyAnimal SpeciesBorrelia Seroprevalence Borrelicidal Effect
DECZBorrelia burgdorferi s.s.Borrelia gariniiBorrelia afzelii
Odd-toed ungulatesEquidaeEquus africanus f. asinus13/1 (8%)2/2 (100%)weak to moderatemoderate to strongmoderate to strong
Equus africanus somaliensis10/1 (10%)1/1 (100%)-*--
Equus ferus caballus5/2 (40%)3/3 (100%)---
Equus ferus ferus-5/5(100%)---
Equus grevyi18/1 (6%)----
Equus hemious kulan12/2 (17%)----
Equus przewalskii98/22 (22%)----
Equus quagga33/9 (27%)8/7 (88%)weakstrongStrong
Equus zebra25/1 (4%)5/4 (80%)weakstrongStrong
TapiridaeTapirus terrestris10/2 (20%)----
RhinocerotidaeCeratotherium simum3/2 (67%)----
Diceros bicornis-7/0 (0%)---
Even-toed ungulatesCervidaeAlces alces alces13/2 (15%)1/1 (100%)---
Cervus albirostris10/1 (10%)----
Cervus canadensis-1/1 (100%)---
Cervus elaphus bactrianus11/0 (0%)----
Cervus elaphus hippelaphus37/0 (0%)----
Cervus eldi thamin10/1 (10%)----
Cervus nippon pseudaxis20/0 (0%)----
Cervus timorensis3/1 (33%)----
Dama dama dama20/0 (0%)----
Elaphurus davidianus14/0 (0%)----
Moschus moschiferus4/3 (75%)----
Rangifer tarandus13/1 (8%)1/1 (100%)---
CamelidaeCamelus ferus f. bactrianus14/1 (7%)----
Lama guanicoe48/3 (6%)1/1 (100%)---
Lama vicugna5/1 (20%)----
SuidaePhacochoerus africanus-1/0 (0%)weakweakWeak
BovidaeAddax nasomaculatus-5/5 (100%)---
Aepyceros melampus6/1 (17%)3/0 (0%)strongstrongweak to strong
Ammelaphus imberbis-2/2 (100%)---
Ammotragus lervia19/1 (5%)6/5 (83%)moderateweakModerate
Antidorcas marsupialis-1/0 (0%)---
Antilope cervicapra16/1 (6%)----
Bison bison14/2 (14%)----
Bison bonasus17/0 (0%)----
Bos gaurus8/1 (13%)----
Bos gaurus f. frontalis4/1 (25%)----
Bos javanicus23/2 (9%)----
Bos primigenius f. Taurus21/2 (10%)2/0 (0%)weakstrongModerate
Boselaphus tragocamelus7/2 (29%)----
Bubalus arnee f. bubalis9/2 (22%)----
Budorcas taxicolor11/3 (27%)----
Capra aegagrus cretica9/1 (11%)----
Capra aegagrus f. hircus17/4 (24%)5/5 (100%)---
Capra caucasica-1/1 (100%)---
Capra falconeri heptneri12/5 (42%)1/1 (100%)---
Capra ibex nubiana6/2 (33%)----
Cephalophus natalensis1/1 (100%)----
Connochaetes gnou-3/1 (33%)weakstrongWeak
Damaliscus pygargus phillipsi-1/1 (100%)---
Eudorcas thomsonii-2/2 (100%)---
Gazella dama9/1 (11%)----
Hemitragus jemlahicus10/0 (0%)----
Hippotragus equinus-1/1 (100%)---
Hippotragus niger-4/3 (75%)moderatestrongStrong
Kobus ellipsiprymnus11/1 (9%)1/0 (0%)moderatemoderate to strongmoderate to strong
Kobus leche-1/1 (100%)---
Naemorhedus caudatus-2/0 (0%)weakmoderate to strongModerate
Nanger dama-5/3 (60%)weak to moderatemoderateModerate
Oreamnos americanus20/9 (45%)2/2 (100%)---
Oryx gazella dammah10/0 (0%)5/3 (60%)moderatestrongweak to strong
Oryx gazella gazella10/0 (0%)2/2 (100%)---
Ovibos moschatus11/8 (72%)----
Ovis ammon f. aries83/8 (10%)5/3 (60%)moderatestrongModerate
Ovis ammon musimon18/3 (17%)----
Ovis dalli3/1 (33%)----
Ovis nivicola1/1 (100%)----
Pseudois nayaur11/0 (0%)----
Redunca redunca14/0 (0%)1/0 (0%)strongstrongWeak
Saiga tatarica31/1 (3%)----
Syncerus caffer caffer17/2 (12%)1/0 (0%)weakweakWeak
Syncerus caffer nanus9/4 (44%)----
Tragelaphus angasii-2/1 (50%)weakweakWeak
Tragelaphus strepsiceros10/0 (0%)2/2 (100%)---
GiraffidaeGiraffa c. reticulate-1/0 (0%)moderatestrongStrong
Giraffa c. rothschildi-2/0 (0%)moderatestrongStrong
CarnivoresFelidaeAcinonyx jubatus-1/0 (0%)weakweakWeak
Crocuta crocuta-1/1 (100%)---
Felis lybica4/1 (25%)----
Felis serval3/1(33%)1/0 (0%)weakweakWeak
Lynx rufus2/1 (50%)----
Panthera leo49/11 (22%)1/0 (0%)weakweakWeak
Panthera leo persica-1/0 (0%)weakmoderateWeak
Panthera onca15/1 (7%)----
Panthera pardus59/8 (14%)----
Panthera pardus orientalis-1/0 (0%)weakweakWeak
Panthera tigris98/2 (2%)----
Puma concolor12/0 (0%)----
UrsidaeUrsus arctos arctos11/0 (0%)----
Ursus maritimus12/0 (0%)----
Ursus thibetanus6/1 (17%)----
CanidaeCanis lupus-4/4 (100%)---
Canis mesomelas-1/1 (100%)---
Lycaon pictus14/0 (0%)2/1 (50%)weakweakWeak
OtariidaeZalophus californianus1/1 (100%)----
PrimatesCercopithecidaeColobus angolensis-1/0 (0%)---
HylobatidaeHylobates lar-1/1 (100%)---
Birds Phoenicopteridae Phoenicopterus roseus-1/1 (100%)weakweakStrong
Struthionidae Struthio camelus-2/0 (0%)weakweakStrong
Reptiles Testudinidae Astrochelys radiata-1/0 (0%)strongstrongStrong
Crocodylidae Crocodylus siamensis-3/0 (0%)weakweakWeak
Pythonidae Python bivittatus-1/0 (0%)strongstrongStrong
DE—Germany, CZ—Czech Republic, * hyphens in the table represent unavailable data in given research.
Table 2. Ticks and tick-borne diseases detected in animals living in zoos and zoo-like establishments.
Table 2. Ticks and tick-borne diseases detected in animals living in zoos and zoo-like establishments.
PathogenAnimal SpeciesTick Species FoundPrevalence (Positive/Tested)CountryReference
TBEVBarbary macaque (Macaca sylvanus)Ixodes ricinus8/284 (2.8%)Germany[72,78]
Markhor (Capra falconeri)I. ricinus1/1 ab* (100%)Czech Republic[20]
Reindeer (Rangifer tarandus)I. ricinus1/1 ab (100%)Czech Republic[20]
Babesia spp.Ocelot (Leopardus pardalis)N/A26/43 ab (60.5%)Brazil[109]
Little-spotted cat (Leopardus tigrinus)N/A9/38 ab (23.7%)Brazil[109]
Margay (Leopardus wiedii)N/A2/4 ab (50%)Brazil[109]
Pampas cat (Oncifelis colocolo)N/A3/5 ab (60%)Brazil[109]
Jaguar (Panthera onca)N/A6/13 ab (46.1%)Brazil[109]
Puma (Puma concolor)N/A2/18 ab (11.1%)Brazil[109]
Jaguarundi (Puma yagouaroundi)N/A6/25 ab (24%)Brazil[109]
Crab-eating fox (Cerdocyon thous)N/A2/39 ab (5.1%)Brazil[109]
Bush dog (Speothos venaticus)N/A8/27 ab (29.6%)Brazil[109]
Maned wolf (Chrysocyon brachyurus)N/A2/2 (100%)USA[111,112]
Reindeer (R. tarandus)N/A1/1 (100%)USA[106]
Babesia odocoileiWapiti (Cervus canadensis)N/A2/30 (6.7%)Canada[98,105]
Reindeer (R. tarandus)speculated Ixodes scapularis12/12 (100%)Canada, USA[24,108]
Red deer (Cervus elaphus) N/A4/144 (2.8%)Canada, USA[98,101,107]
Markhor (C. falconeri) speculated I. scapularis4/6 (66.7%)USA[108]
Yak (Bos grunniens)speculated I. scapularis1/2 (50%)USA[108]
Muntjac (Muntiacus reevesi)speculated I. scapularis1/2 (50%)USA[108]
Babesia venatorumReindeer (R. tarandus)I. ricinus21/141 (14.9%)Germany, Netherlands, Switzerland[32,34,103]
Babesia capreoliReindeer (R. tarandus)I. ricinus7/137 (5.1%)Germany, Netherlands[34,97]
Babesia divergensReindeer (R. tarandus)I. ricinus7/154 (4.5%)Germany, Great Britain[34,104]
Babesia capreoli-likeReindeer (R. tarandus)I. ricinus4/123 (3.3%)Germany[34]
Babesia odocoilei-likeReindeer (R. tarandus)I. ricinus2/123 (1.6%)Germany[34]
Babesia leoGenet (Genetta tigrina)N/A1/2 (50%)Brazil[109]
Theileria spp.Reindeer (R. tarandus)N/A1/1 (100%)USA[120]
Reindeer (R. tarandus)I. ricinus1/123 (0.8%)Germany[34]
Theileria equiTapir (Tapirus terrestris)N/A11/19 (57.9%)Brazil[121]
Theileria bicornisWhite rhinoceros (Ceratotherium simum)N/A2/2 (100%)Australia[117]
Black rhinoceros (Diceros bicornis)N/A1/7 (14.3%)Australia[117]
Cytauxzoon felisOcelot (L. pardalis)N/A7/138 (5%)Brazil[114,122],
Puma (P. concolor)N/A2/9 (22.2%)Brazil[114]
Jaguar (Panthera onca)N/A1/9 (11.1%)Brazil[114]
Lion (Panthera leo)Amblyomma cajennense1/1 (100%)Brazil[115]
Tiger (Panthera tigris)Amblyomma americanum1/1 (100%)USA[123]
Anaplasma phagocytophilumReindeer (R. tarandus)I. ricinus17/123 (13.8%)Germany[33]
Przewalski’s horse (Equus przewalskii)unspecified Ixodid ticks4/4 (100%)USA[26]
Lion (P. leo)N/A1/10 (10%)Italy[130]
Timber wolf (Canis lupus occidentalis)I. ricinus1/1 (100%)Austria[31]
Llama (Lama glama)Ixodes pacificus1/1 (100%)USA[23]
Little-spotted cat (L. tigrinus)N/A4/25 (16%)Brazil[132]
Bush dog (Speothos venaticus)N/A1/27 (3.7%)Brazil[132]
Ehrlichia canisJaguar (P. onca)N/A2/9 (2.2%)Brazil[131]
Ocelot (L. pardalis)N/A3/30 (10%)Brazil[122,132]
Jaguarundi (P. yagouaroundi)N/A5/25 ab (20%)Brazil[131,132]
Little-spotted cat (L. tigrinus)N/A5/39 ab (12.8%)Brazil[131,132]
Margay (Leopardus wiedii)N/A1/1 ab (100%)Brazil[131]
Puma (P. concolor)N/A3/17 (17.6%)Brazil[131,132]
Pampas cat (L. colocolo)N/A1/3 (33.3%)Brazil[131]
Lion (P. leo)N/A2/12 (16.7%)Brazil[132]
Crab-eating fox (C. thous)N/A3/39 (7.7%)Brazil[132]
Bush dog (S. venaticus)N/A5/27 (18.5%)Brazil[132]
Timber wolf (Canis lupus)Rhipicephalus sanquineus13/17 (76.5%)USA[27]
Ehrlichia chaffeensisRing-tailed lemur (Lemur catta)A. americanum7/9 (77.8%)USA[28]
Ruffed lemur (Varecia variegate rubra)A. americanum1/10 (10%)USA[28]
Little-spotted cat (L. tigrinus)N/A3/25 (12%)Brazil[132]
Ocelot (L. pardalis)N/A2/15 (13.3%)Brazil[132]
Puma (P. concolor)N/A2/8 (25%)Brazil[132]
Tiger (P. tigris)N/A2/8 (25%)Brazil[132]
Jaguarundi (P. yagouaroundi)N/A1/19 (5.3%)Brazil[132]
Lion (P. leo)N/A1/12 (8.3%)Brazil[132]
European wolf (C. lupus)N/A1/3 (33.3%)Brazil[132]
Crab-eating fox (C. thous)N/A2/39 (5.1%)Brazil[132]
Rickettsia spp.Lion (P. leo)N/A2/10 (20%)Italy[130]
Theileria spp., A. phagocytophilum and A. bovisSouth African giraffe (Giraffa camelopardalis giraffa)N/A1/1 (100%)China[133]
Coxiella burnetii and A. phagocytophilumLion (P. leo)N/A1/1 (100%)Italy[130]
SFTSVCheetah (Acinonyx jubatus)unspecified Ixodid tick2/2 (100%)Japan[134]
specific data. ab*: antibodies positive; without ab: PCR positive; N/A: No ticks found on the positive animals.
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MDPI and ACS Style

Hrnková, J.; Schneiderová, I.; Golovchenko, M.; Grubhoffer, L.; Rudenko, N.; Černý, J. Role of Zoo-Housed Animals in the Ecology of Ticks and Tick-Borne Pathogens—A Review. Pathogens 2021, 10, 210.

AMA Style

Hrnková J, Schneiderová I, Golovchenko M, Grubhoffer L, Rudenko N, Černý J. Role of Zoo-Housed Animals in the Ecology of Ticks and Tick-Borne Pathogens—A Review. Pathogens. 2021; 10(2):210.

Chicago/Turabian Style

Hrnková, Johana, Irena Schneiderová, Marina Golovchenko, Libor Grubhoffer, Natalie Rudenko, and Jiří Černý. 2021. "Role of Zoo-Housed Animals in the Ecology of Ticks and Tick-Borne Pathogens—A Review" Pathogens 10, no. 2: 210.

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