Ticks of donkeys in central Oromia regional state, Ethiopia

Ticks of donkeys in central Oromia regional state, Ethiopia B. FEREDE 1, B. KUMSA 2, A. BSRAT 1, S. KALAYOU 1 * 1 Mekelle University College of Veterinary Medicine, Po.Box:3189, Mekelle, ETHIOPIA. 2 Addis Ababa University Faculty of Veterinary Medicine, Debrezeit, ETHIOPIA. *Corresponding author: shewit.kalayou@mu.edu.et or skalayout@yahoo.com SUMMARY A cross sectional study was conducted from November, 2008 to March, 2009 with the aim of determining the common prevalent ticks (family: ixodidae) infesting donkeys and associated risk factors in six peasant associations of Ada a and Akaki districts. Donkeys of all age of either sex under the service of Donkey Health and Welfare Project (DHWP) clinic at Bishoftu and Donkey Health and Welfare Project mobile clinic at Dukem, Insilalle, Abusera, Godino and Tulula challo were examined for the presence of ticks. Overall, 144 (32%) donkeys were found infested with at least one genus of ticks and of 144 tick infested donkeys 83 (22.6%) showed skin lesions. Rates of tick infestation in Ada a were higher than in Akaki district (OR=3.358, P=0.012). The figures were 34.5% for the former while 18.6% for the later. Univariate logistic regression analyses of risk factors indicated that district, Peasant Associations (PA), sex, body condition score and months had significant differences and associations with presence of ticks. However, the association was not significant with age. Among the total 579 ticks collected, the relative proportions of the ticks encountered in order of their abundance were Amblyomma (72.5%; 420/579), Rhipicephalus (22.8%; 132/579), Boophilus (4.5%; 26/579) and Hyalomma (0.2%; 1/ 579). Keeping in mind that each tick contributes to the whole of the animal s welfare and productivity, donkey owners and veterinarians should be fully aware of the significant ticks in donkeys. Further study on the vectoral consequences of ticks is advocated. RÉSUMÉ Prévalence des tiques chez l âne en Ethiopie Une étude a été conduite dans 6 associations de paysans des régions d Ada et d Adaki sur la période de novembre 2008 à mars 2009. L objectif était de déterminer la prévalence des tiques infestant les ânes et les facteurs de risque associés. Des animaux de tous ages et sexes ont été examinés pour la présence de tiques. Au total, 32 % des animaux étaient infestés avec au moins un genre de tique et 22 % de ces animaux présentaient des lésions cutanées. La prévalence de l infestation était supérieur dans la région d Ada que dans le district d Akaki. Une analyse des facteurs de risque a montré l influence de la localissation géographique, le type d association professionnelle, le sexe de l animal, l état d entretien. Sur les 579 tiques collectés, les genres observés étaient, par ordre de fréquence décroissante : Amblyomma (72.5 % ; 420/579), Rhipicephalus (22.8 % ; 132/579), Boophilus (4.5 % ; 26/579) and Hyalomma (0.2 % ; 1/ 579). Compte tenu de l impact possible de l infestation des ânes par les tiques sur leur bien être et leur productivité, il est important que les éleveurs et les vétérinaires soient conscients de ce problème. Mots clés : Ada a, Akaki, ânes, Ethopie, ixodidae, tiques, prévalence. Keywords: Ada a, Akaki, donkey, Ethiopia, ixodidae ticks, prevalence. Introduction It is thought that more than half the world s population depends on animal power as its main source of energy (22]. In Ethiopia there are 5.02 million donkeys, 2.75 million horses and 0.63 million mules that account for 37%, 58% and 46% of all donkeys, horses and mules in Africa, respectively [3, 5]. The donkey is more adapted to the terrain geography of Ethiopia than horses and mules. Donkeys in and around the rift valley are used for over fifteen kinds of pack operation including transportation of grains, water, fertilizer, fuel wood and building materials [1]. Despite the great contribution of donkeys to the development of rural and urban economy of Ethiopia, they receive less attention regarding feeding, health and management cares [11,22]. This has resulted in considerably reducing their work output, reproductive performance and working lifetime. Several disease conditions caused by endoparasites and ectoparasites hinder the optimum utilization of donkeys [15]. Among these ectoparasites, ticks are one harmful parasite. For any livestock species, the impact of ticks on animal health can be two fold. These are effects of tick burden as ectoparasites and the effect of diseases transmitted by ticks serving as vectors. As ectoparasites, ticks are responsible for blood loss and irritation [4]. In addition to production losses, tissue damage also provides portal of entry for secondary bacterial infection and for larvae that induce myiasis and tick paralysis due to toxins they release into the blood. In Ethiopia, several tick species of the genera Amblyomma, Boophilus, Haemaphysalis, Hyalomma and Rhipicephalus have been identified in various regions of the country [4, 9, 10, 14, 16, 17, 24]. More than 60 species of ticks infesting both domestic and wild animals have been recorded [10] and 33 of these are known to be most common and are important parasites of livestock [14]. Tick borne diseases transmitted by the major tick species in Ethiopia are anaplasmosis, babesiosis, cowdriosis and benign theileriosis [9, 10]. The most economically important tick-borne diseases, East Coast Fever and acute theileriosis which are caused by Theileria parva and Theileria annulata, respectively and their vectors are not so far reported in Ethiopia. [2, 9]. Despite these docu-

122 KALAYOU (S.) AND COLABORATORS ments, the achievement made on the study of tick and tickborne diseases affecting donkeys in Ethiopia in general is not significant; especially there is paucity of information on ticks of donkeys. Knowledge of tick population dynamics enables to design control strategies that suit the different environment and different animal species. Therefore the objectives of the current study were to establish a baseline data on the common prevalent genera of Ixodidae ticks and explore risk factors associated with tick infestation in working donkeys of two districts of central Oromia Regional State. Materials and Methods STUDY AREA The study was conducted from November 2008 to March 2009 in two different districts of Oromia regional state, namely Ada a (Bishoftu, Godino and Tulula challo) and Akaki (Abu sera Dukem and Insilalle). The study covered donkeys in three Peasant Associations (PAs) of each district. Bishoftu is the main town of Ada a and is located 47 Km east of Addis Ababa at an altitude of 1900 meters above sea level. Geographically Bishoftu lies at 08 44 N and 38 58 E on the escarpment of the Great Rift Valley. Akaki is similar in geography with Ada a and located 20km southeast of Addis Ababa 9.02 8 N and 38.45 8 E. Akaki is located in the central highland plateau at mid altitude on the escarpment of the Great Rift Valley. The topography of the area is marked by the presence of a number of crater lakes. These lakes and the position of the town on the escarpment of the Grate Rift Valley influence the climate of the area. The area experiences a bimodal rainfall pattern with short rainy season from March to May and the long rainy season from June to September. The area has a mean annual rainfall of 1151.6 mm and annual minimum and maximum temperatures of 8.5 C and 30.7 C, respectively and the mean annual humidity is 61.5% [12]. The farmers in the area practice mixed crop-livestock farming system. The area comprises large population of equines, ruminants and poultry. The means of transportation include vehicles, and equids. Horse drawn carts are preferably used for roads that are inaccessible to car at relatively lower charges. STUDY METHODOLOGY Donkeys of all ages and both sexes under the service of Donkey Health and Welfare Project (DHWP) clinic at Bishoftu and DHWP mobile clinic at Akaki, Dukem, Insilalle, Abu sera, Godino and Tulula challo were examined for the presence of ticks. They provide a power source for transportation, draft power and field operation. Most of the owners keep their donkeys in open housing system with stone-paved floor without bedding where animal manure and wasted feed are not regularly cleaned. The available donkey feed resource of this area consists of natural pasture, concentrates and crop residue. SPANA and DHWP, both charity organizations give equine veterinary clinic service within 50 kilometers radius of Bishoftu town. 450 animals admitted to Donkey Health and Welfare Project either for deworming or other maladies were randomly selected and examined for any tick presence. Various risk factors like age, body condition score; skin lesion, district, months and sex were examined for their association with the outcome (tick presence/absence). Body condition of all sampled animals was assessed and recorded during physical examination of the animal as grades 1, 2, 3, 4 and 5 representing for thin, less than moderate, moderate, fat and very fat, respectively. The scoring was based on the method suggested by Marteniuk and Carleton [6]. Age of the selected donkeys was determined by dentition. Donkeys were grouped in to three age categories. Donkeys under two years of age were grouped as young, those in a range of two to ten years were classified as adults, and those beyond ten years were considered as old. These age classes were based on age of first work, productive age and the life span of Ethiopian donkeys [19]. TICK COLLECTION AND PRESERVATION Ticks were collected successfully from donkeys at different predilection/feeding sites after being restrained using various methods such as using strong crushes, by casting down using ropes or by physical handling [13]. Ticks were manually collected by searching on different regions of the animals body. The skin of each study equine was inspected for the presence of ticks. Various predilection/ feeding sites, base of the tail, ear, perianal area, sternum, scrotal area and the belly, were the targeted sites. All stages of ticks, Larvae, nymph, and adults (both sexes) were collected and then, using universal bottles, collected ticks were preserved in 70% ethyl alcohol. Ticks that were not identified at the study site were preserved in 10% formalin and transported to the parasitology laboratory of Veterinary Medicine Faculty in Addis Ababa University, Debre-zeit for species identification. LABORATORY TECHNIQUES FOR TICK EXAMINATION Ticks were identified to species level with aid of Stereomicroscope and binocular light microscope [21]. Ticks were identified into their species level depending up on their morphology and identification structures they have, such as shape of scutum, leg color, body, coxae one and ventral plates (male). DATA ANALYSIS Data collected from field were entered into Microsoft excel spread sheet (Microsoft Crop.). These data were analyzed by descriptive statistics, univariate regression using (SPSS) statistical package for windows version 15 [18]. The prevalence of tick infestation was calculated as the number of positive animals divided by the total number of animals examined and multiplied by hundred [20]. Similarly, prevalence of skin lesion also was calculated by dividing the number of animal observed with skin lesions and total number of animal examined as a denominator. Univariable logistic regression was applied to measure the strengths of the association. The logistic model was checked

TICKS OF DONKEYS 123 for goodness-of-fit using the Hosmer and Lemeshow test. The logistic-regression model was fitted with tick infestation (Present/absent) as the outcome. The model was built using the forward stepwise (conditional) selection procedure by applying the iterative maximum-likelihood estimation procedure and statistical-significance contribution of individual predictors (or group of predictors) to the models tested using the Wald s test and likelihood-ratio test. P<0.05 was taken as significant. Results DESCRIPTIVE DATA A total of 579 ticks were collected of which 89.5% was from Bishoftu, 0.2% from Godino, 6.2% from Tulula challo, 1.9% from Abusera, 1% from Dukem and 1.2% from Insilale. The ticks were identified and found belonging to four genera and six species of the family ixodidae. Ticks infesting donkeys in the study area belong to the genera, Amblyomma, Rhipicephalus, Boophilus and Hyalomma in order of decreasing of abundance. The most common tick species were found to be A. variegatum, R. e.evertsi, R. pulchelus, and Boophilus species. Species of very little abundance include Hyalomma marginatum rufipes and R. muhsame. Analysis of tick developmental stages indicates 52.9%, 42.8% and 0.3% were adults, nymph and larvae, respectively. The overall infestation intensity (total number of ticks per total number of infested donkeys) was calculated as 4.02. The relative abundance of ixodid tick species encountered in various peasant associations, stages and infestation intensity of ticks of the study areas is shown in table 1. TICK PREVALENCE IN WORKING DONKEYS OF SIX PEASANT ASSOCIATIONS (PA) The overall prevalence of tick infestation was recorded as 32% (144/450). Prevalence rates of ticks across the six Peasant Associations are shown in table 2. DIFFERENCE AND ASSOCIATION OF FACTORS AFFECTING PREVALENCE OF TICKS The differences between tick prevalence in donkeys per each risk factor categories as well as their associations are summarized in table 3. During the statistical analyses of all risk factors, the first level of each independent variable was Tick species Peasant Associations Total ticks Tick stage Infestation intensity Bishoftu Godino Tulula Challo Abusera Dukem Insilale No. % L N A N * Intensity ** Amblyomma variegatum 379 1 26 3 5 6 420 72.5 1 219 200 95 4.29 Rhipicephalus. evertsi evetsi 72-1 3 - - 76 13.1-19 57 33 2.3 Rh. muhsame 2-4 2 - - 8 1.4-2 6 4 2 Rh. pulchelus 31-3 - - - 34 6-9 25 13 2.62 Rh. sanguineus 10-2 2 - - 14 2.3 1 3 10 3 4.33 Boophilus species 24 - - - 1 1 26 4.5-19 7 11 2.36 Hyalomma marginatum rufipes - - - 1 - - 1 0.2 - - 1 1 1 Total 518 1 36 11 6 7 579 100 2 271 306 -- Over all 89.5% 0.2% 6.2% 1.9% 1% 1.2% - - 0.3% 46.8% 52.9% 144 4.02 L, larva; N, Nymph; A, Adult ticks; N, Total number of ticks collected; N*, number of donkeys infested with particular tick species. TABLE I : Relative abundance of ixodid tick species encountered in various peasant associations, stages and infestation Intensity of ticks of the study area, Central Oromia regional State, Ethiopia (November, 2008- March, 2009). Peasant Tick Total Intensity * Prevalence associations Absent present (%) Bishoftu 223 113 336 1.54 33.6 Godino 13 1 14 0.07 7 Tulula challo 13 17 30 1.2 30.8 Abusera 33 6 39 0.28 15.4 Dukem 13 3 16 0.38 18.75 Insilale 11 4 15 0.47 26.7 Total 306 144 450 1.29 32% X 2 =19.203, df=5, P=0.002, Intensity- total tick count divided by total number of donkeys sampled in each peasant association. TABLE II : Distribution of the overall tick prevalence in working donkeys of six peasant associations in Ada a and kaliti districts, Central Oromia Regional State, Ethiopia ((November, 2008- March, 2009).

124 KALAYOU (S.) AND COLABORATORS used as a reference category. The result indicated that tick infestation rate was found highest in older donkeys (42%; 57/136), followed by adult donkeys (28%; 81/289) and the rate in young donkeys was found to be 24% (6/25). This difference was not however statistically significant. Higher prevalence of tick was observed in Ada a district (34.5%; 131/380) than that of Akaki (18.6%; 13/70). This was statistically significant (P=0.012). Analyses of tick infestation across the various sampling months indicated a slight increase in tick numbers from November to January, slight decrease in February with a sharp rise in March 2009. This was statistically highly significant (P=0.000) (Table.3). TICK PREDILECTION SITES The distribution of each species of ticks on the host s body is also summarized (Table 4). Belly area and both internal and external ear parts were the sites most ticks were collected followed by the inguinal, perianal areas and hind limbs. 56.9%, 26.7%, 16.4% of A.variegatum ticks were from belly, ear and inguinal areas, respectively. Similarly, 56.6% of R.e. evertsi were from perianal area, 25% (19/76) from ear and 13.2% (10/76) from belly. R.e.evertsi was the only tick species found in hind limb. H. m.rufipes, R.muhsame and R. sanguineus were found only in the belly area. R.pulchelus and Boophilus species were only found in two areas, the ear and belly. Discussion Donkeys harbor myriad infectious and parasitic agents, not all of which have been thoroughly investigated in this animal in Ethiopia. Many authors have contributed to the survey of tick faunas of Ethiopia [14, 22, 23]. But the focus of all of the studies was ticks of cattle, sheep, camel and goats. This study is pioneered in reference to the limited availability of literatures on ticks of donkeys. In the current study, the overall prevalence of tick infestation was found to be 32% with the presence of four genera and six species of Ixodidae ticks. These tick species have been previously reported [4, 10, 14, 16, 17, 24]. A. variegatum (vector of Cowdria ruminantium and Theileria mutans) and Boophilus species (vector of Anaplasma marginale and Babesia bigemina) are the most widespread ticks in Ethiopia [8, 9]. R.e evertsi is also known to occur across different ecological zones of the country serving as a vector for Babesia bigemina in cattle [14]. R. pulchells are confined to semi-arid areas [25]. R.e evertsi and H. m. rufipes have been also reported from cattle, sheep, goat and camel throughout the country [8]. The remaining species occur in limited numbers and have little practical significance to livestock production [9]. The study indicated that the overall mean tick count per donkey was 1.29 (range=0-77). This is relatively smaller Risk Category level Number Prevalence P-value OR 95% C.I. for OR factors Sampled (%) lower Upper District Akaki 70 18.6 Ada a 380 34.5 0.012 3.358 1.308 8.622 P.A. Bishoftu 336 33.6 0.005 Godino 14 7.1 0.051 1.852 0.997 3.439 Tululachalo 30 56.7 0.138 0.205 0.025 1.666 Abusera 39 15.4 0.001 5.272 2.014 13.803 Dukem 16 18.8 0.453 0.628 0.186 2.117 Insilale 15 26.7 0.600 0.635 0.116 3.469 Age Young 25 24.5 0.382 Adult 289 28 0.529 1.179 0.801 2.001 old 136 42 0.235 1.792 0.921 2.364 Sex Female 275 27.6 Male 175 38.9 0.013 0.601 0.402 0.899 Body condition Thin 1 100 0.165 score Less than Moderate 172 33.7 0.538 0.413 0.129 0.697 Moderate 224 33 0.639 0.412 0.126 0.690 Fat 48 18.8 0.037 0.210 0.009 0.422 Very fat 5 40 0.700 0.451 0.201 0.713 Month November 54 13 P<0.001 December 155 24 0.096 2.105 0.877 5.054 January 132 40 0.001 4.505 1.893 10.719 February 50 38 0.005 4.115 1.547 10.944 March 59 48 P<0.000 6.065 2.359 15.591 TABLE III : Summary on results of the univariate logistic-regression analysis of risk factor with dependent presence of ticks in working donkeys of Central Oromia Regional State, Ethiopia (November, 2008- March, 2009).

TICKS OF DONKEYS 125 Species of ticks Predilection site Total Ear Ear belly under tail Hind limb Udder/ count (inside) (outside) (anus area) testicle A.variegatum 38 74 239 - - 69 420 H. marginatum rufipes - - 1 - - - 1 Rh. evertsi evertsi - 19 10 43 4-76 Rh. Muhsame - - 8 - - - 8 Rh. Pulchelus 6 19 9 - - - 34 Rh. sanguineus - - 14 - - - 14 Boophilus species 4 12 10 - - - 26 Total 48 124 291 43 4 69 579 TABLE IV : Feeding preference sites and relative abundance of ticks collected from working donkeys of Central Oromia Regional state, Ethiopia (November, 2008- March, 2009). than the average counts of other species of animals [2, 7]. Coat colour and odour of donkeys might have contributed for the smaller tick burden in donkeys. Further study on host specificity of ticks on donkeys would be interesting. Among the infested donkeys, the overall intensity was calculated as 4.02, highest for A. variegatum and R.e evertsi and lowest for H.m.rufipes. Frequent contact between donkeys and cattle might have contributed to the abundance of these two species. As the present study dealt only with the on-host tick population study, it couldn t clearly show the abundance of two host tick species such as R.e.evertsi, and three host ticks such as A.variegatum which spent some time off their host. Univariate logistic regression analyses of risk factors indicated that district, PA, sex, month and body condition were highly associated with tick prevalence. There was however no significant association with age. The number of ticks and degree of tick infestation of donkeys are influenced by the variation in altitude, among others [2]. Taking Akaki district as a reference category, the odds of tick infestation in donkeys was higher in Ada a than Akaki district (OR=3.358, P=0.012). The apparent variation in tick prevalence between the two districts may not be attributed to their geographical variation. The factor may be explained due to the variation in months of sampling. Tick collection in Akaki was conducted only in November, December and January; however, the procedure was continued in Ada a district in February and March when the short rainy season commences. It has not been possible to draw the seasonality of tick populations for the complete year. However, the result of tick collections at monthly intervals during the period of the study indicated that there was slight increase in tick populations for the first three months, decreased in fourth month and followed by a sharp rises in the last fifth month (March). This may be due to the reason that the onset of the short rainy season in the March has favored oviposition and development of ticks. The study also indicated that the prevalence of tick was higher in males 68 (38.95%) than that of females 76 (27.6%) and the variation was statistically significant (P=0.013). This may be due to the reason that male donkeys in these areas are herded with other domestic livestock and spend at least half a day on grazing unless needed for work. At night they are kept together with other livestock. Female donkeys spend their time largely around homesteads and are better sheltered than the males and hence minimal tick exposure. The infestation of tick was comparable across the different body conditions with prevalence of 33.7% and 33% in less than moderate and moderate condition, respectively. Fat donkeys experience less tick prevalence. Each species of ticks has one or more favored feeding sites on the host, although in dense infestations, other areas of host may be used. Some feed chiefly on the head, neck, shoulders and others in the ears still others also around the anus and under the tail. Immature and adults often have different preferred feeding sites [2]. All species of ticks were found in belly area. The most abundant species in the study areas, A. variegatum, was mostly found in abdominal sites and ear. It was also the only species found in inguinal area. This is inconsistent with our finding that 57.7% (83/144) of tick positive donkeys were presented with skin lesion. This skin lesion was mostly found at belly and on ear areas, where the predilection site of A.variegatum was most frequent. R.e evertsi, R.pulchelus and Boophilus species, were distributed on most parts of the body while R. sanguineus and R.muhsame were often encountered in abdominal regions. A. variegatum and H. m. rufipes were encountered around belly. One weakness of the present study is that it didn t answer the question what diseases these ticks cause. In conclusion, despite the great contribution of donkeys to the development of rural and urban economy of the Ethiopia, tick control in Ethiopian donkeys is considered as a luxury. The over all, result indicated that only few species of ticks are commonly found on donkeys warranting main focus on the dominant ones. Keeping in mind that each tick contributes to the whole of the animal s situation and productivity, it would be advisable that donkey owners and veterinarians should consider tick control as part of the broader improving management and welfare of equines. Further study on the extent of tick-borne pathogens in donkeys is advocated. Acknowledgement We wish to acknowledge the Donkey Health and Welfare Project, Debre- Zeit, for their logistic support during sample

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