The high prevalence of tick infestation (68.2%) and the circulation of TBPs (7.6%) among camels in Saudi Arabia represents a risk to the health and welfare of these animals. Being blood-sucking arthropods, ticks can cause irritation and traumatic injuries to the skin of camels. The damaged skin will adversely affect the energy and water balance of camels in arid environment [44] and also attract flies leading possibly to myiasis infections [45]. The most prevalent tick species identified was H. dromedarii, which is considered as the main species parasitizing dromedary camels [10, 11]. Hyalomma dromedarii is a thermophilic tick usually found in arid and hyper-arid regions [46] with the high prevalence reported from camels in Sudan, Iran, Egypt, Saudi Arabia and Tunisia, with an infection rate ranging between 49–89% [10, 46–49] although it can also infest sheep, goats and horses [50]. This tick species is the principal vector of Theileria spp. of domestic and wild ungulates in Saudi Arabia [8]. The other two species herein identified in camels, H. impeltatum and H. excavatum, usually parasitize cattle and sheep [8, 51] and their finding in camels might be due to the husbandry practices in desert areas where all livestock share common inhabitancy, wandering in nature searching for water sources and grazing land.
The absence of Babesia spp. and Theileria spp. DNA in tested samples agrees with previous studies [13, 15] though these pathogens were diagnosed on some occasions by microscopic examination [23–25]. However, these results do not allow drawing any definitive conclusions about the occurrence of those pathogens in the sampled population, also considering the temporary nature of parasitemia in the blood of infected animals. To date, DNA of Theileria equi, T. annulata, T. mutans, T. ovis and B. caballi have been detected in blood of dromedaries [18, 52–55]. There is limited knowledge on piroplasms specific for camels and due to lack of experimental infections and molecular characterisation, the taxonomic status of some species such as Theileria camelensis [56], Theileria dromedarii [57], Theileria assiutis [58] and Babesia cameli [59] remain unresolved. The detection of H. canis in one camel represents, to our knowledge, the first report of this pathogen among camels, and this could be accounted for by the low host specificity and ubiquitous distribution of H. canis [60] and its vectors (i.e. Rhipicephalus sanguineus (sensu lato). While R. sanguineus (s.l.) was not found on camels in this study, this tick is known to occur on dogs in Riyadh [61].
Among rickettsial organisms, A. platys was the most prevalent pathogen (n = 9, 5.3%), though a much higher prevalence of Anaplasma spp. was detected in previous studies (i.e. 26% from Saudi Arabia [21] and 61% from Nigeria [55]). Anaplasma platys is a parasite with tropism for platelets having a wide host range, primarily being the causative agent of canine cyclic thrombocytopenia [62]. Even though definitive proof of the vector competence of R. sanguineus (s.l.) is currently lacking, this tick species is supposed to be the vector of A. platys [63]. Indeed, the presence of A. platys DNA amplified from R. sanguineus (s.l.) collected from Bactrian camels has been previously reported [64]. Although A. platys was initially considered to be a pathogen of dogs, recent reports support the occurrence of this pathogen in other livestock and humans suggesting a more broader host range for this pathogen [55]. Accordingly, E. canis mainly found in dogs, has been reported in domestic ruminants [65], with some strains diagnosed in dromedary camel of Saudi Arabia [21]. The occurrence of canine pathogens such as A. platys and E. canis in camels can be due to the co-inhabitance of these animals in desert area as well as to the strict affiliation of R. sanguineus (s.l.) to canids and its ability in surviving a large array of environmental conditions [66]. Overall these ecological features give a hint about the possibility of transmission of these pathogens from dogs to camels.
For its zoonotic potential, the retrieval of A. phagocytophilum in camelids is relevant. This pathogen has been mostly diagnosed worldwide in wild roe deer and a wide variety of wildlife fauna [67–69]. In camels, relatively high A. phagocytophilum positivity values have been reported in Tunisia (i.e. 29.2% based on serology) [70] and Iran (34.3% based on PCR) [71]. While it has been demonstrated that several animal species may act as reservoirs of A. phagocytophilum [72, 73], the role of camelids remains to be ascertained. In the same way, the competence of Hyalomma spp. ticks as vectors for this pathogen needs confirmation.
Sequence analysis of the data revealed the circulation of two different STs of A. platys while pathogens like H. canis and E. canis had only one ST. High genetic variability has been already reported within Anaplasma spp. in different hosts from different geographical locations [21, 74]. In the ML tree, two STs of A. platys from camels clustered within those of dogs irrespective of the geographical location, indicating its circulation amongst different animal species. This may occur due to a spillover of A. platys infection from canids to camelids [55]. Moreover, a ST of Anaplasma sp. found herein clustered with a group of Anaplasma spp. sequences from other ruminants from Senegal. This strengthens the possibility of genetic variation and high diversity of Anaplasma spp. The phylogenetic analysis showed that H. canis from camel clustered with those of wild carnivores (i.e. red foxes and of Ruppell’s foxes) in a separate sister clade. Nonetheless, the finding of this parasite in a camel is probably a casual finding in an accidental host.