All cattle surveyed in this study were infested by adult ticks, in both Zamfara and Sokoto States. The generally relatively low degree of infestation, which did not differ significantly between the two States, could be the outcome of (i) the time of the year when the sampling took place (i.e. late dry season, when most tick populations are expected to be less abundant than in the wet season) and (ii) the traditional control practice based on manual removal of ticks, adopted periodically (e.g. once a week) by cattle keepers [8].
The rich diversity of tick species parasitising cattle encountered in this survey is generally in keeping with contemporary reports in Nigeria [8, 9]. As expected for sites in the Sahel, Hyalomma species dominated [51, 54–57]. While it represents the first investigation of this kind for the State of Zamfara, this study confirms the occurrence of five Hyalomma spp. (i.e. H. dromedarii, H. impeltatum, H. impressum and H. trunctatum) which were previously recorded, although in different prevalences, by two surveys carried out on cattle in Sokoto [19, 21].
The presence of such a high relative prevalence of H. dromedarii is remarkable (Fig. 2.I, a-d). Commonly known as ‘the camel Hyalomma’, this tick has a wide distribution in Africa, encompassing arid and desertic regions that are north of the equator, where it is the predominant species parasitising camels [51]. Numerous previous reports demonstrate its ability to infest several hosts including cattle, but not with the relative success observed in this study [54, 58]. In Sokoto, H. dromedarii was the most frequently encountered tick, accounting for almost half the total number of collected ticks (43.7%), suggesting frequent transfer of ticks from camels to cattle and/or that H. dromedarii has adapted itself to parasitise cattle here to a degree not reported elsewhere in its range. The presence of H. dromedarii on cattle in the absence of (frequent) camel contact has indeed been noted previously but only at very low infestation rates [59]. Our findings are in general agreement with those from two previous surveys carried out on cattle from Sokoto, in 2009-10 [19] and 2013 [21], recording H. dromedarii as the second the most prevalent tick species (13.3% and 15.4%, respectively), in both cases after H. truncatum (15.5% and 18.4%, respectively) [19, 21]. Nonetheless, the remarkably higher prevalence documented by the present investigation may be suggestive of adaptation of H. dromedarii towards parasitising cattle which may have occurred in recent times in Sokoto State. Further investigations aiming to verify this hypothesis and assess the potential implication of ecological and climatic factors, would be advisable. Our observation of the dominance of H. dromedarii on cattle in Sokoto mirrors the findings by Lawal et al. [56] and Onyiche et al. [57], reporting H. dromedarii as the most prevalent (46.9%) [56] and the second most prevalent (42.3%) [57] tick species collected in camels from Sokoto. Interestingly, in the very recent survey by Onyiche et al. [57], specimens of H. dromedarii tested positive for the presence of DNA of the Q fever agent Coxiella burnetii. The fact that the dominance of H. dromedarii on cattle was not also observed in Zamfara suggests that the ecological niche it currently occupies in Sokoto does not extend southward within the Sudan savanna of Nigeria and could also be attributable to Zamfara’s smaller camel population compared to Sokoto [59].
In Zamfara, H. rufipes was by far the most abundant tick encountered (Table 2; Fig. 2.II, a-d). This species is the most widespread member of the genus present in Africa and its major contribution to cattle-associated tick fauna has been reported at several sites across this range [55, 60, 61]. It was previously identified in cattle from North-Central (i.e. Plateau State) [8, 9], North-Eastern (i.e. Taraba and Borno States) and North-Western Nigeria (i.e. Kaduna, Kano, Katsina and Sokoto States) [9, 19, 21]. Its veterinary importance is linked to its capacity to act as vector of Anaplasma marginale [62] and Babesia occultans [63]. It is also recognised as an important vector Crimean-Congo haemorrhagic fever (CCHF) virus to humans [51]. Importantly, specimens of H. rufipes collected from camels at slaughterhouses in Kano State, were previously found positive for DNA of Rickettsia aeschlimannii, responsible for a zoonotic spotted fever [66].
Hyalomma impeltatum (Fig. 2.III, a-d) was the second most prevalent tick species (n = 93/254; 36.6%) in Sokoto State; this tick was found in more modest numbers in Zamfara State (n = 14/240; 5.8%) (Table 2). Commonly infesting camels in Northern Nigeria [56, 64], this species was also documented in trade cattle that reached Ibadan, South-Western Nigeria, hailing from the North of the country or neighbouring Chad or Niger [27] as well as in cattle from Sokoto State [19, 21]. The prevalence of H. impeltatum recorded by this survey in Sokoto (i.e. 36.4%) was higher than that previously documented in cattle from the same State (10.1% and 9.4%, respectively) [19, 21], confirming the adaptability of this species to parasitising cattle in areas of sympatry with camels. Like for H. rufipes, specimens of H. impeltatum collected from camels in Kano State were found to harbour DNA of the zoonotic R. aeschlimannii [64].
In this study, specimens of H. truncatum (Fig. 2.IV, a-d) were recorded in cattle from both Zamfara and Sokoto State (Table 2). This tick is known for commonly infesting cattle in Nigeria [8, 9, 15, 16, 19, 21]; its significance is mostly related to its capacity to cause a toxic syndrome (‘sweating sickness’), particularly in young cattle [65] and to the injuries caused by its long mouthparts, especially in the interdigital clefts [51]. Like H. dromedarii, H. truncatum specimens collected from camels from Northern Nigeria (i.e. Sokoto, Kano and Jigawa States) were found to harbour C. burnetii DNA [57].
This study confirms the occurrence of H. impressum in North-Western Nigeria (Fig. 2.V, a-d). Initially documented in trade in Ibadan [27], this tick was previously described in cattle from Sokoto State [19, 21]. The fact that H. impressum was encountered on cattle in this study but not in the two aforementioned surveys on camels from Sokoto [56, 57] may reflect a stronger host-specificity for cattle, although this conclusion is confounded by the low relative abundance of this species on the cattle we observed. Moreover, specimens identified as H. impressum were also encountered in camels in Kano State [56, 64]. Very little is known about the veterinary importance and vectorial competence of this tick species, although some engorged specimens in Ibadan showed to harbour kinetes of ‘Babesia spp.’ [27].
One male specimen of H. marginatum was identified in cattle from Zamfara State. It was morphologically distinguished from the closely related H. rufipes, especially on the basis of the distinctive pattern of grooves on its conscutum (Fig. 2.VI, a-b). Usually reported in livestock across the Maghreb region, Egypt, Sudan and Ethiopia [51], the occurrence of this tick species may be more common that known until now in the Sahel region. In Nigeria, this tick was previously detected in trade cattle probably introduced from neighbouring Chad or Niger [27]. It is however thought of being unable to survive under desert conditions [50], which may explain its absence from cattle surveyed in Sokoto State, in this study as well as in previous ones [19, 21] and suggest that it may be more prevalent during the wet season months. Like H. rufipes, it can be a vector of the zoonotic CCHF virus [51].
Perhaps the most noteworthy encounter among cattle-associated ticks in Zamfara was H. turanicum (Fig. 2.VII, a-b). This species has, to our knowledge, not been reported in Nigeria, or elsewhere in West Africa previously. It is thought to be endemic in the north-east of the continent, and is established in arid, hot parts of southern Africa after accidental introduction [51]. This tick is not known to transmit pathogens to livestock, although it is considered a vector of the CCHF virus to humans [51]. Hyalomma turanicum has a two-host life cycle, with adults typically parasitising wild and domesticated large ruminants and larvae and nymphs feeding on smaller mammals and ground-frequenting birds [51]. The tick has also been reported in Europe, associated with migratory birds using the western European-African flyway [66]. As this flyway embraces Nigeria and large parts of Africa north of the Sahara, it is reasonable to propose that the H. turanicum observed in Zamfara was introduced as a feeding nymph by a migratory bird. As yet to it too early to conjecture if H. turanicum is established in Northern Nigeria; further surveys of cattle and likely hosts of immature life-stages would help clarify this uncertainty. Considering the suitability of this tick species for desert and steppe landscapes [51], climate change-induced desert encroachment in the Sahelian region may potentially favour the establishment of H. turanicum in Northern Nigeria.
A few (n = 7), all male specimens of A. variegatum (Fig. 2.VIII, a-b) were recorded in cattle from Zamfara. The low numbers of A. variegatum recorded in Zamfara, coupled with its absence from cattle from Sokoto State, may be due to the fact that the sampling took place during the late dry season, while the adult population of this tick species tends to peak during the wet season. Accordingly, this tick was previously documented in cattle from Sokoto, surveyed between January and December [19] and February and July [21]. This species is indeed known to be widespread across Nigeria [8, 9, 16, 19, 21], being responsible for the transmission of several bovine TBPs such as E. ruminantium, Dermatophilus congolensis, T. mutans and T. velifera (reviewed in [8]). In this study, however, none of the three A. variegatum specimens screened was positive for Apicomplexan DNA.
One (female) specimen of Rh. (Bo.) decoloratus (Fig. 2.IX, a-c) was also collected from a cow from Zamfara State. Known as the vector of B. bigemina, A. marginale and A. centrale [23], this species is considered the most prevalent boophilid tick infesting cattle in North-Central Nigeria [8, 13]. As for A. variegatum, its low abundance can be due to the seasonality of this tick, peaking during the wet season [8, 16], rather than when this survey took place.
Rhipicephalus (Boophilus) microplus was not recorded in any of the cattle sampled in this study, suggesting that the spread of this invasive tick, likely introduced in Nigeria through cattle from Benin [9] and so far identified in North-Eastern (i.e. Borno, Taraba and Yobe States) [9–11], North-Central (i.e. Kwara State) [9], South-Eastern (i.e. Enugu State) [12] and South-Western Nigeria (i.e. Ogun and Ondo States) [9], has probably not reached the North-West of the country. In Nigeria, indeed, this tick species can be expected to occur mostly in the southern regions, with higher relative humidity and annual precipitation compared to the drier northern States [9].
The preponderance of male rather than female specimens for most tick species collected in cattle from Zamfara State is an accordance with the existing literature (reviewed in [8]). Female ticks are indeed more frequently groomed off by cattle and tend to parasitise them for shorter periods compared to adult males [8]. The detection of more female than male specimens among the ticks collected in Sokoto State can be attributed to the context where the sampling took place. With sampling sites being rather crowded cattle markets (Fig. 1), it is possible that our collection may have somehow privileged female ticks, that are indeed more conspicuous thus more easily identifiable with the naked eye, than male ones.
This study provides the first report of T. annulata in Nigeria. Tropical theileriosis is recognised as one of the most economically important diseases of livestock across North Africa and much of Asia [67], and its presence in SSA, where livestock productivity is already severely compromised by endemic parasites and pathogens [3], is an additional concern. In Africa, T. annulata has so far been detected in eight countries, mostly in the northern (i.e. Morocco, Algeria, Tunisia and Egypt) and eastern part of the continent (i.e. Sudan, South Sudan and Ethiopia) [67], with only Mauritania accounting for the locality records reported so far for West Africa [67–70].
Our detection of T. annulata DNA in ticks collected off 18 (of 35 tested) cattle in three different markets in Sokoto as well as off two (of seven tested) cattle in one village in Zamfara suggests it may be established in North-Western Nigeria. Considering that a significantly greater proportion of ticks and cattle from Sokoto contained T. annulata DNA than in Zamfara, it is likely that the parasite is more prevalent in the former State. That Sokoto is a likely port of introduction, be it recent or not, and circulation of this pathogen, is not unexpected. The State of Sokoto is indeed a major centre for livestock (including camels) trade in the region, attracting farmers and pastoralists not just from North-Western Nigeria, but also from neighbouring Niger and further afield in the Sahel and Saharan regions [71, 27]. The importance of trans-border trade as routes of entry of exotic ticks and TBPs into Nigeria has been established in the South-West of the country [72], with no information being available for the North of the country. Further characterisation of the T. annulata populations detected in Sokoto using, for example, previously described polymorphic markers [73] and comparison of these data with those obtained elsewhere in the parasite’s range, may help pinpoint their provenance.
It is currently unclear if T. annulata has been long-established in North-Western Nigeria or if it is a recent arrival. Indeed, that tropical theileriosis has not been reported before in Nigeria may reflect absence or a low awareness of it as a clinically apparent disease. The latter may also have resulted from endemic stability in the region coupled with low susceptibility of local cattle breeds to clinical disease, as reported elsewhere [74, 75]. Similarly, surveys carried out in cattle Mauritania, during the wet and the dry seasons, did not reveal any clinical case [69], with Zebus in the southern part of the country being found to have high specific antibody titres to T. annulata [68]. Nevertheless, a fatal case of bovine theileriosis was reported in a Friesian cow born in a dairy farm in Nouakchott, originally established with cattle imported from France, where H. dromedarii was the only tick species retrieved [68].
Surveys of local cattle are therefore urgently required to further exploration of the epidemiology of this infection and assess its clinical importance in cattle reared in North-Western Nigeria and potentially in other neighbouring regions. Importantly, the emergence and spreading of resistance to the most widely used theilericidal compound on the market (i.e. buparvaquone) in T. annulata strains circulating in Northern and Eastern Africa [67], further highlights the need for future epidemiological investigations. Moreover, given that the susceptibility of camels to T. annulata has been established and infections appear common elsewhere [76], they too should be surveyed to explore what role they play in the natural cycle of T. annulata in the area. A small survey of TBPs in camels in Sokoto previously detected Theileria species, but not specifically T. annulata [77].
In the present study, five tick species were detected positive for T. annulata DNA, namely H. dromedarii (13/51 tested ticks; 25.5%), H. impeltatum (11/43 tested ticks; 25.6%), H. rufipes (i.e. 3/37 tested ticks; 8.1%), H. truncatum (3/13 tested ticks; 23.1%) and H. impressum (1/9 tested ticks; 11.1%) (Table 3). Of the four Hyalomma species implicated in the transmission of T. annulata in Africa (i.e. H. scupense, H. anatolicum, H. dromedarii and H. lusitanicum) [67], only H. dromedarii was encountered on cattle in this study, and at far greater abundance in Sokoto than Zamfara. Thus, it can be hypothesised that H. domedarii could be the most probable vector of T. annulata in North-Western Nigeria. However, other agro-ecological determinants, such as immature ticks’ host availability and husbandry practices may also underlie the inter-State differences we observed. Due to its capacity to withstand very hot and dry habitats, H. dromedarii is thought to have a strong comparative advantage over other endemic tick African species, in regions where climate change is expected to enhance the environmental aridity [67]. These characteristics, coupled with the vulnerability to climate change of North-Western Nigeria, may cause an increase of the prevalence of theileriosis in cattle from the region, in case T. annulata was only recently herein introduced and if the local vectorial competence of H. dromedarii was confirmed. Indeed, by creating new suitable habitats for H. dromedarii, the expansion of arid areas due to climate change, may lead the infection to spread across North-Western Nigeria, together with its presumable vector.
In Mauritania, H. dromedarii was proposed as the natural vector of T. annulata [68–70], although it was also noticed that the serological prevalence in cattle increased in areas with more diversified tick fauna, suggesting the potential implication of other species such as Rhipicephalus evertsi evertsi [68, 69]. This tick species was previously recorded in cattle in two surveys from Sokoto State (with a prevalence of 2.6% and 5.5%, respectively) [19, 21], as well as from south-eastern (i.e. Oyo State) [78] and eastern regions (i.e. Adamawa State) [79]. Therefore, the potential participation of Rh. e. evertsi in the epidemiology of T. annulata in North-Western Nigeria could not be excluded and should be further investigated. Future studies aiming to assess the occurrence of this tick species in Zamfara, are also advisable, especially considering that, besides Sokoto, the latter borders also with the States of Katsina and Kaduna, where Rh e. evertsi was recently identified in horses [80].
Like in this study, a few (n = 2/30; 7%) partially fed H. rufipes ticks collected from cattle in the Gorgol region in Mauritania, were also found positive for T. annulata by PCR, although at a much lower prevalence compared to H. dromedarii (n = 17/30; 57%) [70]. The vectorial competence of H. rufipes has indeed been demonstrated experimentally through studies on cattle, in which transstadial transmission (i.e. from nymph to adult) occurred [81]. Nevertheless, this tick is regarded as an unlikely vector of T. annulata in field conditions [81], since its immature stages usually parasitise ground-feeding birds [82]. Nymphal stages of Hyalomma impeltatum were also showed to transmit T. annulata in experimental conditions in Sudan [83]. Yet, this tick species is not considered a relevant vector of T. annulata either [83], because its immature stages mostly feed on rodents, hares and birds [84].
Although our study detected T. annulata DNA in several Hyalomma species, all but one specimen were partially fed or near replete, thus results cannot be interpreted as an indication of vector competence. Moreover, the not infrequent detection of T. annulata DNA in multiple ticks infesting the same individual cow underlines also the possible presence of this pathogen in the bovine blood. Interestingly, the only unfed tick specimen that was found positive in this survey was a male H. dromedarii, this being a further suggestion of the possible implication of this species in the transmission of T. annulata in the region. The state of repletion of male specimens of this tick is indeed identifiable through the examination of the position of the subanal plates (in fed individuals they protrude beyond the posterior margin of the body) [51].