Introduction

Animal production is the backbone of the agriculture subsector in Ethiopia, as it is in many other countries in Sub-Saharan Africa.¹ Communities living in Ethiopia’s Selamago district depend on livestock production. Therefore, social, cultural, and economic existence depends on livestock production despite all livestock production constraints.^2,3 Ethiopia has the largest livestock population in Africa, with an estimated 65 million cattle. Goats, sheep, equines, and camels are the main animals produced throughout the country, with cattle, goats, and camels kept dominantly in pastoral areas.⁴ Despite the large quantity of animals, the subsector has low productivity, and hence, money from this sector cannot play a significant part in the country’s economic development.⁵ Inadequate productivity is linked to indigenous cattle’s limited genetic potential, poor nutrition and reproductive performance, high illness incidence and parasite burden (endoparasites and ectoparasites), insufficient management, and inadequate veterinary services.⁶

Ticks are ectoparasites that can transmit infections that cause bovine illnesses. These can cause skin damage, weight loss, mastitis, abortion, and even death, resulting in significant economic losses.^7-10 Ticks are found all across the world, especially in tropical and subtropical areas.^11,12

Amblyomma, Rhipicephalus(Boophilus), Haemaphysalis, Hyalomma, and Rhipicephalus were among the most common tick genera reported in Ethiopia, with more than 60 species capable of infesting and transmitting disease to both domestic and wild animals.¹³ The most prevalent pathogens transmitted by ticks are Anaplasma spp., Babesia spp., and Theileria spp., as well as rickettsia including virus infect several domestic animal species.^14,15 Ticks can also induce non-specific symptoms such as anemia, dermatitis, toxicosis, and paralysis.¹⁶ Ticks can transmit infections to humans, particularly who have close relationships with animals.

Tick infestation in Ethiopia causes significant economic losses via direct infliction on sensitive body parts like the udder and scrotum, which causes skin damage and disease transmission,^17,18 affecting the economies of Ethiopian farmers as well as international markets.¹²

It is critical to keep up research on tick distribution in the area to the level of tick species identifications, which will be transformed into maps to indicate the distribution of species likely to be found and contribute to plan control strategies in the region. Recent research in the Selamago district revealed the presence of 4 tick genera: Amblyomma, Rhipicephalus (Boophilus), Hyalomma, and Rhipicephalus; however, tick species and major affected body sites were not adequately addressed.¹⁹

Despite significant negative impacts on livestock products and productivity due to direct and indirect consequences of tick and tick-borne pathogens, little information is documented in the Selamago district of the South Omo zone. Selamago district is far distance from the center of Southern Nation and Nationalities People Regional State (SNNPRS) Hawassa. Which is one of the districts occupied by pastoral communities, and these populations rely on cattle raising for their livelihood. Livestock moves from one grazing area to another in search of feed. This will provide opportunities to maintain the tick life cycle, especially for 2- and 3-host ticks. Tick harbored livestock disease pathogens are likely to be spread between herds, which is easily maintained by close contact at any time. There is a need for appropriate strategies for the management of tick and tick-borne diseases, and this requires up-to-date information on the prevalence and distribution of tick species on different hosts, particularly cattle. The objectives of this study was to understand the tick population in the study area, identify tick species, and associate risk factors with the prevalence of tick infestation.

Material and Methods

Study area description

The study was conducted in the South Omo zone of Selamago district. The study district is located 870 km southwest of Addis Ababa and 507 km from Hawassa, the capital of Ethiopia and the Southern Nations and Nationalities People Regional State (SNNPRS), respectively. The study area lies between 6°19′ and 7°10 N latitude and 15°12 and 22°25′ E longitude, with a total land coverage of 451.12 km² and an altitude range of 600 to 2560 m.a.s.l. The area receives bimodal rainfall, in which the long rainfall season occurs from March to June. The short rainfall season is from August to October. The annual average temperature of the area was recorded at 29°C, with a range of 20°C to 37.5°C.²

Selamago district is geographically bordered from the south by Nyangatom district and from the west and north by the Omo River. Whereas from the northeast by Gamo Gofa and from the east by Basketo and Bako Gazer districts, and tributaries of the Mago River. This separates Selamago district from Bena Tsemay; the Mago River defines part of the boundary with Bako Gazer. The administrative center of Selamago is Hana Town, shown in Figure 1.

Figure 1.

Map of Selamago district located under SNNPRS region of Ethiopia.

According to the Selamago district Agricultural Bureau’s annual report of 2022 on livestock population records, the cattle population is about 408 000, sheep about 21 600, goats about 33 200, equines about 1525, and poultry about 52 035.

Results

Overall prevalence of tick population and associated risk factor

In the present study, 384 cattle were examined for the prevalence and identification of ixodid ticks. Out of 384 cattle examined, 262 cattle had one or more ticks with an overall prevalence of 68.2%. Univariable logistic regression analysis result that showed different output between the prevalence of tick infestation with assumed risk factors (age, sex, kebele, and body condition score). There was a statistically significant association (P < .05) with age and sex. A higher tick infestation was seen in the adult age group with a prevalence of 76.2% than in the young with a prevalence of 49.5%. Whereas females had a prevalence of 75.5% which was greater than males with prevalence of 60.6%. There were no statistically significant (P > .05) differences between Kebele and body condition score (Table 1). Those significant variables were checked by stepwise backward analysis using multivariable logistic regression. Age and sex categories showed statistically significant in multivariable logistic regression. Hosmer-Lemeshow goodness of fit model evaluation suggested that estat gof χ² = 4.43 with P = .035 and estat class evaluation correctly classified 67.71% as well as Receiver operating characteristics (ROC = 0.6679) for best fitted model shown in Table 2.

Table 1.

Prevalence and univariable logistic regression of ixodid tick and its associated risk factors.

Table 2.

Multivariable logistic regression analysis of age and sex risk factors.

A total of 579 ixodid ticks were collected from the 262 cattle, which were identified in 4 genera and 7 different species. The genera of ticks that were encountered in the study period were Amblyomma, Rh.(Boophilus), Rhipicephalus, and Hyalomma, with proportions of 64.9%, 15.7%, 15.1%, and 4.3%, respectively, as shown in Table 3.

Table 3.

Proportion of ixodid tick genus identified in Salamago district.

Tick species identified and their distribution on the skin of cattle

Among tick species identified in this study, Amblyomma spp., particularly A. variegatum, was the predominant tick species that was collected (187 with a prevalence of 32.2%), followed by A. gemma and A.lepidum while Hyalomma truncatum showed the least prevalence (25 count with prevalence of 4.3%) as shown in Table 4. Some of tick species captured for the purpose of this study shown in Figure 2.

Table 4.

Proportion of ixodid tick species identified in the study area.

Figure 2.

Specimens that shown tick species observed during study period.

In this study, the most frequently observed ticks were in the perineum (30.4%) region, followed by the udder/scrotum (24.5%), dewlap (14.3%), belly, head/neck, ear (14.3%), and leg (9.1%), as shown in Table 4. A soft and hairless region looks more preferred by ticks to attach to (Table 5).

Table 5.

Distributions of ixodid ticks and their proportion on different predilection site of animals body.

Three species of Ambylomma (A. lepidum, A. variegatum, and A. gemma) were identified predominantly in the udder/scrotum, followed by the dewlap, perineum, belly/back, legs/tail, and head regions. Whereas Rh.(Boophilus) decoloratus predominantly attaches around the dewlap, belly/back, legs/tail, udder/scrotum, heads, ears, and perineum regions sequentially. Hy. truncatum preferred the dewlap, head/neck, and perineum shown in Table 6. A high proportion of ticks were observed in the perineum, udder, and scrotum, followed by the dewlap region, regardless of tick species identified during study period.

Table 6.

Proportion of ixodid tick species identified in different predilection site on the body of cattle.

Out of the total ticks collected 365 (63.1%) were male and 214 (36.9%) were female ticks (Table 7). The ratio shows more male were recovered than female tick. The difference between sexes were statistically significant (P < .05).

Table 7.

Observation on ixodid tick male to female ratio in the study period.

Discussion

Studies indicate that different tick species reported in Ethiopia in various agro-climatic and ecological zones of the country. A systematic review using 35 published articles showed about 19 tick species under the genus Amblyomma, Rhipicephalus (Boophilus), Rhipicephalus, Hyalomma, and Haemaphysalis reported in various domestic animals in Ethiopia during the period of 2001 up to October 30, 2020.²⁴ Recently published articles from Gondar, Eastern Hararghe, and Selamago support the current and previous studies finding in Ethiopia, where Amblyomma is the predominant genus.^19,25,26 The overall prevalence of tick populations in the Selamago district was significantly (P < .05) higher compared to non-infected ones. The tick species identified were the same as those reported in various parts of Ethiopia. This finding was comparable with Kebede et al,²⁷ who recorded a prevalence of 69% in Lalo Assabi District, West Ethiopia. Study reports of 61.98% and 61.5% prevalence were recorded in the Humbo and Hetosa districts, respectively, in the SNNPRS and Eastern Arsi zones.^14,28 However, it was higher than the report from Holetta and Bench Maji zone, with an overall prevalence of 25.6% and 27.3%, respectively.^29,30 The difference could be associated with various factors, such as the season of study, whether it was after the wet season when arthropods are populous or during the dry season, that significantly affect the tick population in a given area. The agro-climatic condition of the study area also matters in the distribution of tick infestations. The length of observation could also affect the prevalence; in a longitudinal study, the tick population could vary within the study period, whereas in a cross-sectional study, for instance, a point prevalence at that time is explained. The fact that the current study is a cross-sectional study might be the reason for the discrepancy in the tick population among other similar studies’ finding.²³ In the same study district, higher tick population counts were observed in the wet season than in the dry season.¹⁹ However, the current study was limited to one season and was not possible to compare between seasons. It is stated that agro-climate associated with temperature and rainfall significantly affects tick survival.²³

The present study showed a statistically significant difference (P < .05) in the prevalence of tick infestation between females and males. This finding was in agreement with reports from Pakistan^31,32 and Colombia,³³ reported that female cattle had a significantly higher tick burden than males. However, the finding disagree with another study, which reported a higher tick infestation in male than females animals.^14,34 Management differences between females and males were explained as a factor in closed experimental research in Colombia. However, in Pakistan and Egypt, such a management factor wasn’t explained like in the Selamago district, where cattle were kept in a communal grazing system regardless of their sex. The prevalence difference between sexes is difficult to explain in terms of biology though statistically significant. Hence the difference is not biologically plausible and therefore, the difference might be by chance.

Statistics showed that the prevalence of ticks varied by age group (P < .05). Adult cattle had a higher tick infestation than young cattle, and similar differences were reported in other similar studies. It stated that a higher proportion of tick was observed in adult cattle than in young cattle.^31,33,35,36 This higher proportion of tick infestation in adults may be due to outdoor management and the long-distance movement of adult animals to search for feed and water when compared to younger animals, especially calves that remain around the homestead and are less exposed than adult cattle. It was also suggested that the grooming of calves and the smaller surface area of animals may be factors in the lower tick burdens.³²

There was no significant difference between the body condition score in this study and previous observations in the same area.¹⁹ A significantly higher prevalence was observed in poor-body-conditioned animals than in medium- and good-body-conditioned animals.³⁷ High prevalence in body-wasted animals is associated with low refraction to tick infestation, whereas animals with good body condition showed reasonable defense capacity against the infestation.³³

Moreover, a relatively high tick infestation was recorded at Marsiyoa compared to Geyo and Hanna Kebele. A slight difference in tick infestation was observed in both body condition scores and among kebeles in this study, but it was not statistically significant (P > .05). A study in Colombia, indicated the higher-live-weight animals had a higher tick burden³⁵; this might be confounding with age group, where adult animals have a higher live weight than young animals. In addition, as the animals get older and older, they might suffer from tick burden because of compromised immunity as their age increases.

Seven species of ticks, with respective prevalences, Amblyomma variegatum (32.3%), Amblyomma gemma (17.6%), Amblyomma lepidum (15%), Rhipicephalus (Boophilus) decoloratus (15.2%), Rhipicephalus pulchellus (10.6%), Rhipicephalus evertsi evertsi (5%), and Hyalomma truncatum (4.3%), were identified during the study period. The finding is in agreement with reports from other studies. Among the most commonly reported tick genera in Ethiopia, Amblyomma species are predominantly distributed in different regions of Ethiopia,^38-42 in the study areas of Nekemte, Hararghe, Asella, Awassa, Mizan Teferi, and Jimma. The second most predominantly distributed tick species is under the genus Rhipicephalus, with the maximum incidence reported in Gamo-Gofa, Bale and Southern Sidama; accordingly.^43-45

Although Amblyomma and Rhipicephalus ticks are predominant in many parts of the country, Rh. (Boophilus) and Hyalomma ticks have also been reported significantly. A high prevalence (55%) was reported in Hawassa.⁴⁶ This difference is probably due to different climate conditions.

The tick populations are significantly affected by climatic changes, which affect the rate of tick populations on the ground, host resistance, and biological enemies.^16,23 Studying ticks on livestock under their natural conditions without any control measures is important to understand the host-parasite relationship and the variation of tick populations in different agro-ecological zones.

Rhipicephalus (Boophilus) decoloratus was the second most abundant tick species (15.2%) identified in the present study. Most other studies have reported this tick species as the second most abundant tick infestation.^28,37,47,48 Although there is a prevalence difference from place to place, it is associated with climatic differences, as in Rh. (Boophilus). decoloratus is abundant in humid highlands and sub-highlands that receive more than 800 mm of annual rainfall.⁴⁹

Rh. pulchellus was found to be the third most abundant tick, with a prevalence of 10.3%. It is reported as the most prevalent tick species on camels in Eastern Ethiopia, on small ruminants in the eastern part of Ethiopia, and on cattle in the Borena zone in the Oromia region. The present finding was higher than Haramaya Eastern Hararge, which reported 6%.⁵⁰ R. evertsi evertsi was the other tick species identified in the study area with a prevalence of 5%; however, the prevalence was lower than 21.5% in Bako, Western Ethiopia.³² Belew and Mekonnen³⁶ reported a prevalence of 29.3% in and around Holetta and an equivalent prevalence of 30.5% in and around Asossa.⁵¹ The native distribution of Rh. evertsi evertsi in Ethiopia is related to middle-high dry savannas and steppes. In association with zebra and ruminants, it was reported that this species did not show specific preferences for a particular altitude, rainfall zone, or season.,⁴⁹ but ticks more prefer large animals like cattle and others than small animals.²⁴

With a prevalence of 4.3%, Hy. truncatum was found to be the least abundant tick species collected in this study. This finding was higher than the 0.9% prevalence.⁴⁸ The high frequency of this tick species in the Selamago district may be attributable to the fact that Hy. truncatum is generally found in arid parts of tropical Africa with annual rainfall ranging from 250 to 650 mm, where this ecology is more common in Selamago than in central Ethiopia.²⁴ The low incidence in Ethiopia’s central highlands may be due to considerable rainfall.⁴⁹

Tick infestation in different parts of the animal body shows that the perineum region, followed by udder/scrotum and dewlap had a high proportion of tick burden sequentially. The back, belly, head, and neck body regions showed the lowest tick burden. A longitudinal study findings corroborated this current study, where the perineum region had a higher tick burden than the belly region.^33,52 Other studies have shown that the lowest number of ticks were observed around the eyes, neck, and chest,⁵³ which is in line with the current findings. Ticks prefer hidden and warm anatomical zones on the animal’s body. Therefore, a suitable environment for their survival might be the reason ticks were populous under the tail in the perineal region and between the lower flank of the udder and the scrotum. Similarly, the hind legs, udder, abdomen, forearm, and rear are more exposed to grass and hence more accessible to tick infestation.³¹ The length of grass where the animals graze, whether the grazing style is rotational or confined to a single restricted grazing location influence tick burden in various body parts of the animal’s.

Male ticks outnumbered female ticks in the current study by a ratio of 1.7:1. This study discovery of a higher number of male ticks is consistent with earlier research.^46,54 The finding is biologically plausible because male ticks stay longer on the host than female ticks. This is because of the wide scutum, or shield, at the back of the abdomen in males, that doesn’t allow them to engorge blood sufficiently at one time and will not drop in the first blood feeding, unlike female ticks.⁵⁵ Similar findings were reported in Pakistan,³² where male tick counts were higher and their species identified, whereas immature and engorged female ticks were difficult to count and identify because of morphological deformity. This might be fully engorged female ticks drop to the ground to lay eggs, and some identification traits are obscured, while males tend to stay on the host to continue feeding and mating with other females. In addition, host grooming removes semi-engorged females more easily than males.^46,56

Conclussion and Recommendations

In this study, ticks were found to be widely prevalent, and 4 tick genera and 7 species were identified in the study area. A. variegatum was the most prevalent tick species found in the study area. The perineum was also the most tick infested body area, followed by the udder, scrotum, and dewlap. Appropriate tick control program taking the findings of this study into account should be designed and implemented in the study area. Further researches addressing the economic and public health significance of the identified ticks are recommended.