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Abstract

Background and objective: Ixodid ticks are serious obstacle to development and utilization of animal resource in tropical countries like Sudan. Over 70 species of tick are prevalent in the Sudan in diverse ecological zones. The aim of this study was to provide a baseline data on tick species infesting cattle in the Northern State, Sudan as a prerequisite to design tick control policy in the state as well as the whole country.

Materials and Methods: This study was conducted in April 2017 and included seven provinces of the state. Total body tick collection (n=1,098) was carried out from 365 heads of cattle. Tick identification to the genus and species level was carried out as well as statistical analysis using two-way ANOVA.

Results: Nine tick species of two genera, Hyalomma and Rhipicephalus, were identified. The genus Hyalomma represented 82% of the collected ticks. Hyalomma rufipes was the most common tick species (48.5%) followed by Rhipicephalus praetextatus (14.9%), H. anatolicum (14.4%), H. excavatum (12.8%), H. dromedarii and R. sanguineus (3.4% each), H. impeltatum (2.2%), H. marginatum (0.46%) and the least prevalent tick species was R. evertsi evertsi (0.09%). The prevalence of tick infestation significantly varied within the age groups for H. anatolicum, H. rufipes and H. excavatum. The mean tick infestation was found to be independent on breed and sex of the animals.

Conclusion: It is concluded that there were nine ticks species distributed in the State. Among these species is H. anatolicum, which is the vector of two vital diseases, bovine tropical theileriosis and malignant ovine theileriosis. Thus, tick control strategy, and creation of awareness among animal breeders on the problem associated with tick infestation are recommended.

Introduction

Ticks are destructive and obligatory blood sucking parasites, found in most if not all the countries of the world. They parasitize reptiles, birds and mammals [1]. Ticks cause blood loss, inflammation and irritation of the skin, stimulate hypersensitive allergic reactions; and they may cause a toxic reaction in the host, complicated by paralysis (called “tick paralysis”). They are important vectors of diseases affecting both humans and animals [2].

This is the second study on the distribution of tick infesting livestock in the Northern State of Sudan since the 1950s. The first study on ticks in the Northern State of the Sudan was done by Hoogstraal in 1956 who identified 11 tick species: Hyalomma excavatum, H. dromedarii, H. impeltatum, H. rufipes, H. marginatum, H. impressum, H. detritum, H. truncatum, Rhipicephalus evertsi evertsi, R. sanguineus and R. pretextatus in the Northern Provinces (currently River Nile and Northern States). All subsequent tick surveys were performed in other areas of Sudan. Eleven tick species infesting cattle in River Nile, Central, Western and Eastern parts of the Sudan were identified [3]. These were Amblyomma lepidum, A. variegatum, Hyalomma anatolicum, H. dromedarii, H. impeltatum, H. truncatum, H. rufipes, Rhipicephalus decoloratus, R. evertsi evertsi, Rhipicephalus sanguineus group and R. praetextatus. H. dromedarii, H. impeltatum, H. anatolicum, H. truncatum, H. rufipes, R. praetextatus and R. sanguineus were identified in camel in River Nile State [4]. In Sennar State Amblyomma lepidum, H. anatolicum, H. truncatum, R. decoloratus, R. camicasi, R. evertsi evertsi, R. guilhoni and R. muhsamae were identified [5].

The most significant cattle tick in the country (above 10 latitude) is Hyalomma anatolicum, the vector of Theileria annulata and T. lestoquardi the causatives of tropical theileriosis in cattle and malignant ovine theileriosis in sheep, respectively [6-8]. Ticks of Amblyomma variegatum and A. lepidum transmit Ehrlichia ruminantium, among sheep, goats and cattle [9,10], while Rhipicephalus decoloratus and R. annulatus are the main vectors of bovine babesiosis [11]. This study was conducted with the objective of elucidating tick species infesting cattle in Northern State of the Sudan.

Materials and Methods

Study area

The Northern State shares boundaries with four Sudanese states (Khartoum, River Nile State, North Kordofan, and North Darfur State) in addition to Egypt and Libya. The total livestock population of Sudan in the year 2014 is estimated to be about 105.8 million: 30.2 million cattle, 39.8 million sheep, 31.0 million goats, and 4.8 million camels. Cattle population in the Northern State in the same year was estimated to be 256,624 [12]. This study was conducted in seven provinces of the Northern State: Halfa, Dalgo, Borgig, Dongola, Golid, Deba, and Marawi (Figure 1).

Tick collection

The survey was conducted during April 2017. The surveyed infested animals were mostly present in the agricultural areas of the River Nile banks in both east and west side of the river, in addition to the islands. A total body tick collection was made on 365 infested cattle. The collected ticks were transferred into a glass bottle containing 70% ethyl alcohol for preservation and brought to the laboratory for identification. Information such as date and place of collection, age, sex and breed of the host were recorded at the time of collection [13].

Tick identification

The ticks were identified morphologically under a dissecting microscope at Department of Entomology and Ticks, Central Veterinary Research Laboratory, Khartoum, Sudan [12,14].

Statistical analysis

Data collected on ticks were subjected to an appropriate general linear model (GLM) procedure using the Statistical Analysis System (SAS) package. These data include the number of ticks collected, the county where collection was carried out, as well as breed, age groups and sex of cattle from which ticks was collected. The SAS was used to perform two-way analysis of variance (ANOVA) while mean separations were performed using the Ryan-Einot-Gabriel-Welsch (REGW) multiple range test [15].

Figure 1: Study area showing map of Sudan and in the right Northern State, with sample collection sites.

Results

Prevalence of tick species in the Northern State

A total of 1,098 ticks were collected from the infested cattle. Generally, two tick genera, Hyalomma and Rhipicephalus, and nine species were identified from the seven study areas (Figure 2-4). The genus Hyalomma (82%) was more prevalent than the genus Rhipicephalus (18%) in the State. Hyalomma rufipes was the most common tick species (48.5%) followed by R. praetextatus (14.9%), H. anatolicum (14.4%), H. excavatum, (12.8%), H. dromedarii and R. sanguineus (3.4% for each), H. impeltatum (2.2%), H. marginatum (0.46%) and the least prevalent tick species identified was R. evertsi evertsi (0.09%) (Table 1).

Figure 2: Distribution of Hyalomma anatolicum in Northern State, Sudan during April 2019.

Figure 3: Distribution of Hyalomma rufipes in Northern State, Sudan during April 2019.

Figure 4: Distribution of Rhipicephalus evertsi in Northern State, Sudan during April 2019.

Distribution of tick species in the seven provinces

The mean total numbers of ticks per head of cattle at the different location are summarized in Table 2. The highest mean (4.08±0.38) of the number of ticks identified was recorded at Dongola Province, while the lowest mean (1.70±0.17) was recorded at Deba (Table 2). The mean number of H. anatolicum (1.05±0.21) was significantly different in Dongola compared to all other provinces. The same result was reported for H. excavatum (1.58±0.28) and H. impeltatum (Table 2). While the mean number of H. rufipes (2.84±0.37) was significantly different in Dalgo. On the other hand, no significant difference was observed in the mean number of Hyalomma dromedarii and Rhipicephalus sanguineus in seven provinces (Table 2).

The mean tick infestation significantly varied with the age of the animals for H. anatolicum, H. rufipes and H. excavatum. The young calves (<1 years) was found to carry significant higher number of H. anatolicum (0.65±0.12) and H. excavatum (0.65±0.20) than the older cattle (1-3 years and > 3years) (Table 3). With regards to H. rufipes, the highest significant number of ticks (1.65±0.13) was report in the older cattle of >3 years old (Table 3). On the other hand, breed and sex of cattle were found to have no significant effect on the mean tick infestation (Table 3).

Discussion

This is the first time in over 60 years that a study on the distribution of tick species in the Northern State was carried out. All other reported surveys in northern Sudan were performed in River Nile State and southward provinces. Although this survey was carried out in a very limited time frame, nine tick species of both medical and veterinary importance were found to occur in the Northern State of Sudan. These species were H. rufipes, R. praetextatus, H. anatolicum, H. impeltatum, H. excavatum, H. dromedarii, H. marginatum, R. sanguineus and R. evertsi evertsi. Twelve tick species were identified in the Northern provinces of the Sudan [14]. These tick species were: Amblyomma exornatum, H. dromedarii, H. excavatum, H. impeltatum, H. impressum, H. marginatum, H. scupense, H. rufipes, H. truncatum, R. evertsi evertsi, R. praetextatus and R. sanguineus. He also reported in Kordofan the occurrence of H. dromedarii, H. excavatum, H. impeltatum, H. impressum, H. marginatum, H. rufipes, H. detritum, R evertsi evertsi, R. praetextatus and R. sanguineus. H. impeltatum was identified in Kordofan [16]. H. anatolicum, H. dromedarii, H. truncatum, R. evertsi evertsi, R. praetextatus R. sanguineus were identified in Khartoum State [17]. The occurrence of H. anatolicum, R. evertsi evertsi was reported in Khartoum State [18]. H. anatolicum, H. dromedarii, H. rufipes and R. evertsi evertsi were collected from Khartoum State [19].H. anatolicum, H. dromedarii, H. impeltatum, H. rufipes, R. evertsi evertsi and R. sanguineus were identified on cattle in Khartoum State [20]. H. anatolicum H. dromedarii R. decoloratus, H. impeltatum, H. truncatum, H. rufipes, R. evertsi evertsi, R. praetextatus and R. sanguineus were identified from cattle in River Nile State [3]. H. impeltatum, H. dromedarii, H. rufipes, H. truncatum, R. evertsi evertsi are the tick species infesting cattle and sheep in North Darfur [21]. In study, similar tick species to those found in the above-mentioned states was found (Khartoum, River Nile State, Kordofan, and North Darfur). This may be due to the fact that these states share boundaries with the Northern State, and that animals move freely among these States. 

The ticks identified in this study are known to be xerophilic species that can survive well in the arid and harsh environment of Northern State [22]. Immature H. rufipes ticks do not feed on cattle but on birds, while adults feed on larger animals including cattle. The high prevalence and wide distribution of this tick species in the present study is indicative of the availability of immature host species throughout the Northern State [23]. On the other hand, H. anatolicum are well adapted to manmade environment and this may explain its high prevalence and wide distribution in the State [24]. The differences noted in the geographical distribution of ticks and the infestation rates in this study may be related to local ecological differences such as abundance and species of domestic and wild animals, climate and the vegetation cover that exist in a particular area. Other tick spp might have been absent or were present numbers below the detection limit of the current study. 

Finally, we recommend that a large scale longitudinal seasonal survey must be carried out in the whole country with emphasize on Northern State, to update the information concerning the prevalence and distribution of ticks among the livestock.

Conclusion

It is concluded that there were nine ticks species distributed in the State. Among these species is H. anatolicum, which is the vector of two vital diseases, bovine tropical theileriosis and malignant ovine theileriosis. Thus, tick control strategy, and creation of awareness among animal breeders on the problem associated with tick infestation are recommended.

Authors contribution

The present study was a part of an ongoing DFG research project which includes study design, collection of tick samples, identification of tick species and statistical analysis, preparing, and drafting the manuscript. M.T.E. identified tick species and drafted the manuscript, K.M.T. helped in samples collection, A.E. contributed in tick identification and drafted the manuscript, S.M.H. carried out the statistical analysis, D.A.S. contributed in samples collection and drafted the manuscript, J.A., P.-H.C. and A.M.E. were the conceived of the study providing supervision, funds and manuscript preparation. All authors read and approved the final manuscript.

Significance Statement

This study discovered that cattle in Northern State are infested with nine tick species and provided the baseline date for ticks infesting cattle in Northern State of Sudan that can be beneficial for farmers and policy maker and relevant authorities to design a proper and cost effectiveness control strategy for tick control in the state. Since to the best of our knowledge no similar study was conducted in the study area. This study will help the researchers to uncover the critical areas of tick infestation in Sudan that many researchers were not able to explore. Thus, a new theory on tick control may be arrived at.

Acknowledgements

The authors would like to thank Dr. Selma Kamal, Tsetse Department, Central Veterinary Research Laboratory for preparing the maps. This study was supported by Deutsche Forschungsgemeinschaft (DFG) project ‘Molecular epidemiology network for promotion and support of delivery of live vaccines against T. parva and T. annulata infection in Eastern and Northern Africa’ (AH 41/7-1).

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