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. 2025 Mar 29;11(3):e70165. doi: 10.1002/vms3.70165

Tick Species Infesting Livestock in Three Bioclimatic Areas of Senegal: Bioecology, Prevalence of Tick Infestation, Associated Categorical Factors and Crimean‐Congo Haemorrhagic Fever Virus Infection

Aliou Khoule 1,✉, Déthié Ngom 1, Mouhamet Faye 1, Ousseynou Sene 2, Aminata Badji 1, Elhadji Ndiaye 1, Gamou Fall 2, Ibrahima Dia 1, Mawlouth Diallo 1, Diawo Diallo 1,✉
PMCID: PMC11955016  PMID: 40159441

ABSTRACT

Background

Crimean‐Congo haemorrhagic fever (CCHF), a disease of medical and veterinary importance in several countries including Senegal, is transmitted by ticks or exposure to infected body fluids. Severe human cases of CCHF were recently observed across Senegal suggesting modification of the endemicity area and the tick fauna.

Objective

This study aims to investigate some aspects associated with the bioecology of ticks infesting livestock and their infection with CCHF virus (CCHFV) across three bioclimatic areas of Senegal.

Methods

Ticks were collected between October 2020 and November 2022, from randomly selected cattle, goats and sheep in the Sahelian, Sudano‐Sahelian and Sudanian zones. They were screened for CCHFV RNA by RT‐PCR.

Results

A total of 3632 animals were examined, and 35.3% (95% CI: 33.8–36.9) were found tick‐infested. The overall tick infestation rate was 81.7% (95% CI: 78.1–84.9) in cattle, 30.3% (95% CI: 28.2–32.5) in sheep and 24.1% (95% CI: 21.8–26.5) in goats. TIR differed per age, gender, host species and bioclimatic area. Overall, 7734 ticks belonging to 12 species and 3 genera were collected. The most abundant species included Rhipicephalus evertsi (32.7%) and Hyalomma impeltatum (20.1%). CCHFV was detected in 6 of the 1709 tested pools with an overall minimum infection rate (MIR) of 0.8‰. Infected ticks (H. impeltatum and H. rufipes) were collected mainly from the anogenital areas of sheep and cattle in the Sahelian and Sudano‐Sahelian zones.

Conclusion

These updated data on ticks and CCHFV vectors in Senegal will be useful for the prevention and control of tick‐borne diseases.

Keywords: bioclimatic areas, cattle, CCHFV, goats, infestation, Senegal, sheep, ticks

Ticks were collected between October 2020 and November 2022, from cattle, goats and sheep in the Sahelian, Sudano‐Sahelian and Sudanian zones, and tested for CCHFV infection.

A total of 3632 animals were examined and 35.3% (95% CI: 33.8–36.9) found tick‐infested. CCHFV was detected in six tested pools with an overall minimum infection rate of 0.8‰. Infected ticks (H. impeltatum and H. rufipes) were collected mainly from the anogenital areas of sheep and cattle in the Sahelian and Sudano‐Sahelian zones.

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1. Introduction

Ticks, chelicerate arthropods of the class Arachnida (Camicas et al. 1998), are vectors of major impact on animal and human health. Ticks transmit a large number of pathogens to animals and humans, including over a hundred viruses, among theme Crimean‐Congo haemorrhagic fever virus (CCHFV) (Perez‐Eid and Gilot 1998). CCHFV is an arbovirus (genus: Nairovirus, family: Bunyaviridae) transmitted to humans and various animals (sheep, goats, cattle, birds etc.) by Ixodidae ticks, in particular Hyalomma genus. The virus is transmitted also to humans by direct contact with blood or tissues of infected humans or viremic livestock. Infection is asymptomatic in animals, although it causes viremia lasting from 2 to 15 days (Camicas, Wilson, and Cornet 1991). In humans, infections are usually benign but some cases could progress to severe diseases with 5%–40% fatality rates (Bente et al. 2013). CCHF has a wide geographic distribution, cases have been reported in over 30 countries across Africa, southeastern Europe, the Middle East and western Asia (Al‐Abri et al. 2017; Flusin et al. 2010; Hoogstraal 1979). The virus has been responsible for numerous epidemics and sporadic cases in many parts of the world. In West Africa, epidemics have been reported regularly in Mauritania (Schulz et al. 2021), bordered by northern Senegal, the circulation of the virus has been recently noted both in humans and animals in Senegal's neighbours countries (Maiga et al. 2017). Over the past two decades, nine African countries have reported their first human cases of CCHF (Temur et al. 2021). The presence of CCHFV in Senegal was reported since the 1970s, with isolations of the virus from eight tick species (Camicas, Wilson, and Cornet 1991). In contrast to Mauritania, until very recently, only few sporadic and benign CCHF cases were recorded in Senegal (Camicas et al. 1994; Nabeth et al. 2004). High seroprevalence of domestic animals (cattle, sheep and goats) in Senegal was also only high in northern part of the country, one of the areas highly favourable for Hyalomma ticks development, then gradually declining to zero towards the south (Wilson et al. 1990). Between 2021 and 2022, several severe human cases of CCHF were observed in more than five outbreaks in the northern, eastern, western and central Senegal (Mhamadi et al. 2022), suggesting dramatic modification of areas endemicity and basic data on biodiversity and bioecology of tick fauna collected before the drought of the 1970s (Morel 1969). During that time, 15 species (genus Hylomma, Rhipicephalus, Amblyomma, Boophilus and Ornithodoros) were recorded in domestic animals in the Sahelian, northern Sudanese, southern Sudanese and Guinean savannah zones of West Africa. The Sahelian and northern Sudanian domains were dominated by species of Hyalomma genus, while the southern Sudanian and northern Guinean domains were dominated by species of Amblyomma and Rhipicephalus (Boophilus) genus. Longitudinal studies carried out by Gueye et al. (Gueye, Mbengue, and Diouf 1994; Gueye et al. 1987, 1993) investigated the biodiversity and population dynamics of ticks in Senegal during the drought period. These studies showed a reduction of tick‐specific diversity and population of the major CCHFV vectors. A return to normal rainfall in the 2000s (Gaye 2017) has inevitably contributed to the change and revitalization of the herbaceous stratum, a key factor in pastoral ecosystems and the habitat of animals such as ticks. One of the direct consequences of climatic and vegetation changes on ticks could be qualitative (change in terms of diversity, through installation or disappearance of species) and quantitative (through increase or decrease in density) (Fryxell et al. 2015; Gueye et al. 1989). Despite all these changes, little recent work has been done on tick infestation in livestock and CCHFV infection of ticks and livestock in Senegal. This study aims to estimate the prevalence of tick infestation, CCHFV infection in ticks, species diversity, trophic preference and risk factors associated with tick‐infesting cattle, sheep and goats in three bioclimatic areas of Senegal.

2. Materials and Methods

2.1. Study Areas

The study was carried out in three bioclimatic zones of Senegal. These are Sahelian, Sudano‐Sahelian and Sudanian zones (Figure 1). Sahelian zone is located in the north of the 400 mm isohyet. It is characterized by a long dry season lasting 8–9 months. This is the driest part of the country, although the outskirts of the river valley are more or less spared. Temperatures range from 22.6°C to 40.5°C, with an average of 28.9°C. The main activity remains livestock rearing (including the majority of cattle, sheep and goats in the country), despite the rapid deflagration of herbaceous stratum weakened by overgrazing. As a result, livestock breeders make periodic transhumance movements towards the south and centre of the country.

FIGURE 1.

FIGURE 1

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Map showing the three bio‐climatic area and sampling sites (modified from Sylla, Souris, and Gonzalez (2021)).

The Sudano‐Sahelian zone is located between 600 and 1000 mm isohyets, which illustrate a north‐south rainfall gradient. It is a transition zone at the interface between the dry Sahel and the humid south. Temperatures range from 26°C to 39°C, with an average of 29°C. The area is characterized by tannes, estuaries, shrub savannah and tree savannah. The main productive sectors in the area are agriculture, livestock breeding and salt production. Livestock farming is characterized by the existence of two traditional techniques: pastoral breeding based on transhumance and sedentary breeding confined to the village territory. The major livestock species are sheep, followed by goats, cattle and horses.

Sudanian zone is characterized by rugged terrain interspersed with plateaus and valleys, which are the main farming areas. Sudanian zone has a diverse flora and vegetation, with several types of plant formations: the main ones being steppe, savannah, open forest, gallery forest and marshy grasslands. This area is one of the rainiest in the country, with at least of 1300 mm/year and a rainy season lasting around 6 months. Temperatures are generally high, with maxima ranging from 34°C to 42°C and minima from 21°C to 25°C. Relative humidity can exceed 97% between August and October. Extensive livestock rearing is practised with animals left to roam. In this zone, high pressure from tse‐tse fly (trypanosomiasis vector) limits livestock farming to such an extent that only Ndama bulls, dwarf sheep and goats can live in infested areas. The majority of livestock do not make transhumance movements, as they live in the country's wettest zone (Kanh, Sokouri, and Dieng 2019). In this bioclimatic zone, cattle, sheep and goats are the major livestock species.

2.2. Tick Collection and Identification

Ticks were collected between October 2020 and November 2022 from cattle, goats and sheep after informed consent from the farm owners had been obtained. Sample collections were organized monthly (seven in the Sudano‐Sahelian zone, eight in the Sahelian zone and nine in the Sudanian zone). During each visit, an average of 16 animals were selected from each herd for the 227 herds visited, of which 98 were in the Sahelian zone, 80 in the Sahelo‐Sudanian zone and 49 in the Sudanian zone. The animals visited (982 sheep, 621 goats and 70 cattle in the Sahelian zone; 454 sheep, 283 goats and 327 cattle in the Sudano‐Sahelian zone; 338 sheep, 438 goats and 119 cattle in the Sudanian zone) came from extensive and semi‐extensive farms, characterized by irregular application of prophylactic and therapeutic measures. Over 99% of the animals are native breeds. Each individual was carefully screened for ticks by inspection of the whole body divided into seven anatomical regions (ears, dorsal, baleen/abdomen, legs, anogenital, tail and feet). Animal age was estimated by dental examination and grouped into two categories: 05–18 months for young and > 18 months for adults. Ticks were removed manually from the animal with forceps and kept in labelled Nunc tubes. Labelling included collection area, date, host animal, gender and age, and site of attachment on the host. Samples were transported to the laboratory in dry ice or liquid nitrogen. Ticks identification was based on morphological characters, using the Hoogstraal (Hoogstraal 1996) and Walker (A. R. Walker et al. 2003) identification keys. Then, ticks were pooled on a chill table and stereomicroscope by monospecific groups of 1–30 individuals according to date and locality of collection, gender, status, animal host, attachment site and state of feeding.

2.3. Virogical Test for CCHF Detection by RT‐PCR

Ticks were handled in a Biosafety Level 3 (BSL‐3) laboratory, and we also worked in biological safety cabinets with unidirectional airflow and filtration. The tick pools were each placed in a 2 mL tube containing three metal beads and 1 mL of cell culture medium consisting of L‐15 (Gibco BRL, Grand Island, NY, USA) and 20% cold foetal serum (FBS). This mixture was automatically ground using the Tissue Lyser (Qiagen) for 2 min at a frequency of 30 Hz/s and then centrifuged at 10,000 rpm at 4°C for 5 min. After centrifugation, the supernatant was filtered using a 0.20‐µm filter (Sartorius, Göttingen, Germany), collected in a CryoTube (Thermo Scientific) using a 1 mL syringe (Artsana, Como, Italy) and stored at −80°C. Subsequently, 140 µL were used for each tick sample for RNA extraction. RNA was extracted from the tick supernatant using QIAamp RNA Viral kit (Qiagen GmbH, Heiden, Germany) according to the manufacturer's recommendations. The RNA was eluted in 60 µL of AVE buffer and stored at −80°C until use. Detection of CCHFV was performed using the AmpliSens CCHFV‐FRT PCR kit (AmpliSens, Bratislava 47, Slovak Republic) according to the manufacturer's recommendations. A total of 10 µL of RNA was added to a 15 µL reaction mixture consisting of 12.5 µL of the buffer, 4 µL of nuclease‐free water, 1 µL of each primer, 0.5 µL of the probe and 1 µL of the enzyme. The qRT‐PCR was performed on CFX96 (Biorad, Biorad Laboratories, Marnes‐La‐Coquette, France). The cycling conditions were 50°C for 30 min and 95°C for 15 min, followed by 5 cycles of 95°C for 10 s, 54°C for 30 s and 72°C for 15 s, and finally 45 cycles of 95°C for 10 s, 50°C for 30 s (where signal acquisition was performed) and 72°C for 15 s. The signal of the CCHFV cDNA amplification product was detected in the channel for the JOE fluorophore. This RT‐PCR method was previously extensively described (Weidmann et al. 2018).

2.4. Statistical Analysis

All data were entered, in MS Office Excel 2016; data were analysed using R software (R Core Team 2016), version 4.2.2. Fisher's exact test was used to compare tick infestation rates (TIR; number of tick‐infested animals/total number of animals inspected × 100) according to categorical variables (age, gender, host species and origin) and the minimum infection rates for CCHFV (MIRs; defined as the number of positive pools/total specimens of ticks tested × 1000) with p < 0.05 considered significant. In addition, a 95% confidence interval for the prevalence of tick infestation was calculated using a binomial distribution.

Biodiversity indices (Shannon–Weiner index, species richness) were used in this study to quantify biodiversity heterogeneity in the study area and hosts. Shannon–Weiner index is calculated using the following formula:

H′=−∑i=1Spiln(pi)

  • H': Shannon biodiversity index

  • i: a species in the study environment

  • S: species richness

  • pi: proportion of a species i in relation to the total number of individuals (N) in the study area or host, calculated as follows:

  • p(i) = ni/N

The relative abundance of each tick species was calculated as the total number of that tick species collected on a given vertebrate host type or in a given area/the total number of ticks collected on that host species or in that area × 100. The relative abundance for a sampling attachment site was calculated by dividing the number of ticks collected at that site by the total number of ticks sampled × 100.

3. Results

3.1. Tick Infestation Rates

A total of 3632 animals including 516 cattle, 1774 sheep and 1342 goats were examined. Over 99% of these animals were native breeds. Host numbers and tick infestation rates are shown in Table 1. The average TIR of the livestock studied was 35.3% (n = 1283/3632, 95% CI: 33.8–36.9), with variations across host species, age, gender and bioclimatic zone. The tick infestation rate was higher in cattle (81.7%, 95% CI: 78.1–84.9) than in sheep (30.3%, 95% CI: 28.2–32.5) and goats (24.1%, 95% CI: 21.8–26.5) (p < 0.0001). Sheep were statistically more infested than goats (p < 0.0001). Overall infestation rates varied also among bioclimatic zones, with the highest rate in the Sudano‐Sahelian zone (61.5%, 95% CI: 58.4–64.4), followed by Sahelian (27.6%, 95% CI: 25.5–29.8) and Sudanian (18.7%, 95% CI: 16.2–21.4) zones (p < 0.0001 for all pairwise comparisons).

TABLE 1.

Tick infestation rate on livestock according to age, gender, zone and type of host, Senegal, 2020–2022.

Total collected Positive Negative
Categorical variables n % n % 95% CI n % 95% CI p‐value
Prevalence 3632 100 1283 35.3 33.8–36.9 2349 64.7 63.1–66.2
Age, months
Young 593 16.3 170 28.7 25.1–32.5 423 71.3 67.5–74.9
Adults 3039 83.7 1113 36.6 34.9–38.4 1926 63.4 61.6–65.1 < 0.0001
Gender
Male 639 17.6 197 30.8 27.3–34.6 442 69.2 65.4–72.7
Female 2993 82.4 1086 36.3 34.6–38.0 1907 63.7 61.9–65.4 0.01
Zone
Sudanian 895 24.6 167 18.7 16.2–21.4 728 81.3 78.6–83.8
Sahelian 1673 46.1 462 27.6 25.5–29.8 1211 72.4 70.2–74.5
Sudano‐Sahelian 1064 29.3 654 61.5 58.4–64.4 410 38.5 35.6–41.5 < 0.0001
Type of host
Goats 1342 37 323 24.1 21.8–26.5 1019 75.9 73.5–78.2 < 0.0001
Sheep 1774 48.8 538 30.3 28.2–32.5 1236 69.7 67.5–71.8
Cattle 516 14.2 422 81.7 78.1–84.9 94 18.2 15.0–21.9
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Note: p < 0.05 is statistically significant. n: number of specimens.

Abbreviation: CI, confidence interval.

Analysis of tick infestation rates according to categorical variables for each host species showed that adults were more infested with ticks than young in cattle (94.0%, 95% CI: 91.1–96.0 vs. 39.1%, 95% CI: 30.3–48.7; p < 0.0001) and in goats (25.8%, 95% CI: 23.3–28.4 vs. 12.6%, 95% CI: 8.3–18.7; p = 0.0002) but not in sheep (29.6%, 95% CI: 27.3–32.0 vs. 33.9%, 95% CI: 28.6–39.5; p = 0.16). Females were found more infested with ticks than males in sheep (34.1%, 95% CI: 41.6–36.6 vs. 15.2%, 95% CI: 11.7–19.5; p < 0.0001) and in goats (27.0%, 95% CI: 24.4–29.7 vs. 11.0%, 95% CI: 7.5–15.8; p < 0.0001), but there are no significant differences in cattle (82.5%, 95% CI: 78.1–86.2 vs. 80%, 95% CI: 72.5–85.9; p = 0.6). Among bioclimatic zones, the highest rate was observed in Sudano‐Sahelian followed by Sahelian and Sudanian zones for sheep (Sudano‐Sahelian: 48.2%, 95% CI: 43.6–52.9; Sahelian: 29.7%, 95% CI: 26.9–32.7 and Sudanian: 8.0%, 95% CI: 5.4–11.5; p < 0.0001) and goats (Sudano‐Sahelian: 59.4%, 95% CI: 57.7–69.6; Sahelian: 17.1%, 95% CI: 14.2–20.3 and Sudanian: 11.2%, 95% CI: 8.5–14.6; p < 0.0001). However, in cattle, the difference was not significant (p = 0.3), although the TIR was higher in the Sahelian (91.4%, 95% CI: 81.6–96.5) followed by the Sudano‐Sahelian (81.6%, 95% CI: 76.9–85.6) and the Sudanian (76.5%, 95%CI: 67.6–83.5) zones. The variables having a statistically significant effect on tick infestation were gender and bioclimatic zone for sheep, age and bioclimatic zone for cattle, and age, gender and bioclimatic zone for goats.

3.2. Biodiversity and Species Richness

According to Shannon–Wiener index, the results for species diversity (Table 2) showed high species diversity in the study areas. However, the highest diversity was observed in the Sahelian zone (H' = 1.6), followed by the Sudano‐Sahelian zone (H' = 1.4), and the lowest species diversity was observed in the Sudanian zone (H' = 1). Species richness was equal between the Sudanian and Sahelian zones (nine species). Tick diversity and species richness were also calculated according to host, and the results showed identical species richness in the different hosts (11 species). Measurements of the Shannon–Wiener index revealed greater species diversity in all the hosts studied, with the highest correlation with cattle (1.8), followed by sheep (1.7) and goats (1.4).

TABLE 2.

Abundance, species richness and Shannon diversity index of tick populations in the different areas and host, Senegal, 2020–2022.

Tick effect Relative abundance (%) Specific richness (S) Shannon index (H′)
Areas Sudanian 1407 18.2 9 1
Sahelian 2950 38.1 9 1.6
Sudano‐Sahelian 3377 43.7 7 1.4
Hosts Cattle 3580 46.3 11 1.8
Sheep 1215 15.7 11 1.7
Goats 2939 38 11 1.4
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3.3. Relative Abundance of Tick Species by Host and Area

A total of 7734 collected ticks were morphologically identified into 3 genera and 12 species as follows: R. evertsi (32.7%), H. impeltatum (20.1%), A. variegatum (10.7%), H. truncatum (10.0%), H. rufipes (9.8%), R. geigyi (6.6%), R. sulcatus (4.7%), R. guilhoni (2.7%), R. decoloratus (2.2%), R. musahmae (0.4%), R. lunulatus (0.04%) and H. impressum (0.04%).

Relative abundance of tick species according to host and collection area is summarized in Figure 2. R. evertsi was the second most dominant species in the Sahelian zone and the most abundant in the Sudano‐Sahelian zone, with relative abundances of 26.9% and 51.4%, respectively. This species was absent from the Sudanian zone, and 75.6% of its population was collected from small ruminants (sheep, goats). H. impeltatum, the most represented species in the Sahelian zone with a relative abundance of 35.8%, was largely collected from cattle (65.2% of the total), and was not recorded in the Sudanian zone. A. variegatum and R. geigyi were the two most abundant species in the Sudanian zone with relative abundance 54.1% and 36.5%, respectively, and were collected from all three hosts, but their abundances were comparable in small ruminants. These species were not recorded in the Sahelian zone, nor in the Sudano‐Sahelian zone for R. geigyi. H. truncatum and H. rufipes were the only species collected in all three bioclimatic zones. Their respective relative abundances were higher in the Sahelian zone (12.9%, 7.2%) and the Sudano‐Sahelian zone (10.3%, 14.5%) than in the Sudanian zone (3.1%, 3.4%). The total numbers of these two species were collected almost entirely from cattle and sheep. R. sulcatus and R. guilhoni were specially collected in the Sahelian zone with a relative abundance of 9.1% and 6.9%, respectively, but they mainly infested sheep and goats. R. musahmae and H. impressum were collected only in the Sahelian zone in small numbers. The last species (R. lunulatus) was only present in the Sudanian zone on small ruminants (goats and sheep).

FIGURE 2.

FIGURE 2

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Relative abundance of tick species per host and per area, Senegal, 2020–2022.

3.4. Tick Attachment Sites According to Host

Ticks were collected mainly in the anogenital region (cattle: 63%; sheep: 56.2%; goats: 45.1%), followed by the ears (goats: 39.7%; sheep: 30.5%) and the dewlap/abdomen (cattle: 23.9%).

The analysis of tick species attachment sites shown in Figure 3 showed that A. variegatum was most frequent in the dewlap/abdomen of cattle and sheep, with proportions of 66.9% and 32.9%, respectively, but in goats, it was found mainly on the ears (62%). The species H. rufipes and R. evertsi were mainly found in the anogenital region of the various hosts; this observation was made for H. truncatum in cattle and goats, but in sheep, it was mainly found in the tail.

FIGURE 3.

FIGURE 3

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Preferential attachment sites of the five main tick species collected from cattle, sheep and goats, Senegal, 2020–2022.

3.5. Viral Detection in Ticks

Of the 1709 pools tested (1–30 individuals per pool), 6 were positive for CCHFV (Table 3), including 5 from the Sahelian zone, collected from sheep (1 pool of H. rufipes, 2 pools of H. impeltatum) and cattle (2 pools of H. impeltatum). Only one pool of H. rufipes collected from cattle in the Sudano‐Sahelian zone was infected, while all ticks from the Sudanian zone were negative, and no positive ticks were collected from goats. Positive ticks were collected in the anogenital region (n = 5; 83.3% of positive pools) and on the feet (n = 1; 16.7%). The MIR of CCHFV was 0.8‰ for the total number of ticks collected. The MIR of H. impeltatum was higher in sheep (4.3‰) than in cattle (3.8‰) in the Sahelain zone. There was no statistically significant difference in MIRs (p‐value > 0.05).

TABLE 3.

Ticks species found naturally infected with Crimean‐Congo haemorrhagic fever virus in the different areas and hosts, Senegal, 2020–2022.

Area Ticks species/host Number of ticks tested Positive pools/total pools tested MIRs 95% CI
Sahelian H. impeltatum
Sheep 467 2/103 4.3 0.5–15.4
Cattle 528 2/67 3.8 0.5–13.6
H. rufipes
Sheep 83 1/21 12.0 0.3–65.3
Sudano‐Sahelian H. rufipes
Cattle 48 1/48 20.8 0.5–110.7
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Note: MIRs: minimum infection rates × 1000.

Abbreviation: CI, confidence interval.

4. Discussion

Up‐to‐date data on the vector fauna (including specific diversity, relative abundance, prevalence of tick infestation, trophic preference and fixation sites according to hosts and bioclimatic zones) are among the essential factors in tick control and prevention of tick‐borne diseases, particularly in Africa including Senegal, where these diseases are becoming of growing public health importance.

Tick biodiversity, abundance and associated factors of infestation on domestic ruminants have been poorly studied in West Africa (Biguezoton et al. 2016). In Senegal, recent data on tick infestation are limited to a few surveys carried out in a circumscribed area with a small sample size (Biguezoton et al. 2016; Dahmani et al. 2019). The average prevalence of tick infestation observed in this study (35.3%) is lower than that in studies carried out in July 2021 (53.1%) (Badji et al. 2023) and September 2022 (52.1%) (Ngom et al. 2024) on a smaller number of animals (720 and 236, respectively) in a rainy season when ticks are more active in Senegal. It is comparable to that observed in Mali (37.8%) and Iran (39.0%) in domestic ruminants (Monfared, Mahmoodi, and Fattahi 2015), but lower to the 78.3% infestation rate reported in ungulates (goats, sheep, cattle and buffalo) in Pakistan (Rehman et al. 2017). The difference in infestation rates could depend on the variation in the application of prophylactic measures and the bioecology of tick species, which is closely linked to climatic conditions and the specific animal breeding model of each country.

This study shows an infestation rate in cattle (81.8%) comparable to those obtained in Adamaoua (94.7%) in Cameroon (Mbebanga Sassa et al. 2016) but higher than that observed in the Sahel region, northern Burkina Faso (43.7%) (Adjou Moumouni et al. 2022). The prevalence of tick infestation is also higher in cattle than in small ruminants (sheep and goats), which is in agreement with previous studies (Rehman et al. 2017). This difference can be explained by the farming methods used for cattle and small ruminants (Mbebanga Sassa et al. 2016), age (cattle are globally older), and size of animal body. Indeed, in Africa, cattle move slowly over long distances in search of pasture (thus increasing their probability of contact with ticks), whereas sheep and goats generally stay around villages, where they are less exposed. The greater skin surface area and attractiveness of cattle compared to small ruminants could also explain the difference in tick infestation rates (Rehman et al. 2017).

The difference in tick prevalence between zones observed in this study could be linked to climatic and ecological differences. In fact, the geographical distribution of ticks and the population levels of the species are dependent on climatic factors (Gueye et al. 1989). The latter can fluctuate from one area to another or from one period to another, resulting in variations in the distribution of tick species and their abundance.

Infestation rate by gender revealed a higher prevalence of tick infestation in females than in males for small ruminants. Similar results have been reported in previous studies on sheep and goats in Africa and Asia (Rehman et al. 2017). The higher infestation rate in females compared to males could be linked to lower immunity and greater stress (pregnancy and lactation), making them more susceptible to tick infestation (Sutherst et al. 1983). In addition, males of small ruminants are kept in herds for shorter periods than females, as they are more prized for economic (sold for religious and family ceremonies) and dietary needs. Furthermore, they benefit from special care (regular grooming and manual tick removal) reducing their level of tick infestation (Rehman et al. 2017). Unlike small ruminants, male and female cattle have comparable infestation rates. These data are consistent with the results of previous studies (Lotfi and Karima 2021). In fact, male cattle are kept as long as females in herds, and receive no special care compared with male small ruminants.

The higher rates of tick infestation in adult cattle and goats observed in this study are in accordance with the works carried out in Cameroon, Algeria and Iran (Monfared, Mahmoodi, and Fattahi 2015; Mbebanga Sassa et al. 2016; Elfegoun et al. 2013). This observation may be due to the lower immunity and longer travel distances (in search of food) of adults, as opposed to juveniles, increasing their likelihood of infestation by ticks (Mooring et al. 2000). No significant difference was observed between the infestation rates of young and adult sheep. This result is in line with the work of Mollong et al. (2017) and Khan et al. (2022) and inconsistent with Shahid et al. (2021).

According to the Shannon diversity index, there is a very high diversity of ticks infesting animals in the three bioclimatic zones. Out of the 15 tick species documented on ruminants in Senegal (Gueye, Mbengue, and Diouf 1994; Gueye et al. 1987, 1993), we collected 12 species. This species richness is higher than that observed in data reported from Mali and Burkina, respectively, 6 and 5 (Adjou Moumouni et al. 2022; Diarra et al. 2017). However, the number of species in our sample is also low compared with the 33 known in Senegal (Mediannikov et al. 2010); this could be explained by the only sampling method used (direct capture on the host) and a limited choice of hosts (cattle, sheep and goats). Previous cross‐sectional studies carried out in the same geographical zones showed the same diversity (Gueye, Mbengue, and Diouf 1994; Gueye et al. 1987, 1993). But changes were noted in the distribution of species in the different bioclimatic zones compared with the previous studies. The heterogeneity of specific diversity in the different zones could be due to the specific bioecological requirements of each species, as previously indicated by Morel (1969). Indeed, the absence or new reporting of a given tick species in an area would be linked to transhumance and new ecological conditions that would authorize the establishment of this species. The bioecology of the species present in our sample has been addressed by previous studies (Morel 1969; Sylla, Souris, and Gonzalez 2021; Sylla et al. 2008). Our study showed that for the most abundant tick species collected, the main attachment sites varied by the host. Indeed, the main attachment sites were the anogenital region and the tail for Hyalomma and R. evertsi, while these sites were more diversified for A. variegatum. Whatever the attachment site, ticks were mainly found on well‐vascularized parts of the body where there is little or no hair to facilitate blood meal intake (Bourdeau 1993).

R. eversi was the most abundant species in our collection, with a relative abundance of 32.7%, this predominance was observed in a previous study in Senegal (Dahmani et al. 2019). According to Morel (1969), the distribution range of R. evertsi in West Africa lies between isohyets of 400 and 1000 mm. This is in agreement with our observations, indicating its absence of the Sudanian zone, where annual rainfall exceeds 1000 mm (Gueye et al. 1993). In our study, this species was collected in the Sahelian (with a relative abundance of 26.8%) and the Sudano‐Sahelian zones (51.4%). The Sudano‐Sahelian bioclimatic area is considered as the most favourable for this tick development, where its population is clearly increasing compared with previous studies (Gueye, Mbengue, and Diouf 1994). In West Africa, R. evertsi is absent on wild ungulates (J. B. Walker, James, and Ivan 2000) and has a predilection for sheep as shown in this study as well as others (Morel 1969, Mollong et al. 2017). Whatever the animal species considered, the anogenital area was the main attachment site for R. eversi, in agreement with the results of Gueye, Mbengue, and Diouf (1994). This tick was not found to be naturally infected with CCHFV in our study, contrary to what was observed in 2021 (Badji et al. 2023) and Zeller et al. (1997), and its vector competence was demonstrated (Faye, Fontenille, et al. 1999).

The Sahelian tick H. impeltatum is the second most abundant species in our sample, with a relative abundance of 20.1%, the most represented species in the Sahelian zone (35.8%), this result was widely shared by other authors (Morel 1969, Sambou et al. 2014; Badji et al. 2023). Once restricted to the Sahelo‐Saharan region (Gueye et al. 1989), this species has currently the same distribution as R. evertsi. The absence of H. impeltatum in the Sudanian zone in this study and that of Gueye et al. (1993) suggests that this species is only adapted to the arid environment. Just like our results, the preference of this species for cattle is well known (Gueye et al. 1987; Sambou et al. 2014). H. impeltatum was naturally infected with CCHFV in this and many other studies in Senegal. H. impeltatum had the highest numbers of CCHFV infected (four pools) compared with other tick species of the same genus (H. rufipes: two pools). However, the MIRs of CCHV for H. impeltatum were higher in sheep than in cattle, which were more heavily tick‐infested. Domestic animals, especially sheep, have been shown to be asymptomatic carriers of the virus (Spengler, Bergeron, and Rollin 2016), acting as reservoirs of human infection via body fluids or infected ticks. The involvement of H. impeltatum in CCHFV transmission has been demonstrated experimentally (Camicas et al. 1994; Dohm et al. 1996; Spengler, Bergeron, and Rollin 2016).

The species A. variegatum, known as the Senegalese tick, was found in the Sudano‐Sahelian (1.9%) and Sudanian (54.1%) zones in agreement with the statement that this species only found in regions receiving at least 500 mm of annual rainfall (Morel 1969). In southern Senegal, a high abundance of this tick was reported by Mediannikov et al. (2010). Our results showed that the overall infestation caused by this tick on sheep and goats is much lower than that observed on cattle. Nevertheless, A. variegatum far outweighs the other species besides R. geigyi collected from small ruminants in the Sudanian zone. This observation is consistent with previous studies (Gueye et al. 1993). However, its immatures could be ubiquitous (Stachurski, Barré, and Camus 1988). The variety of attachment sites observed could be related to the divergent preferential location between preimaginal and imaginal stages (Farougou, Kpodekon, and Tassou 2007). All virological tests for the detection of CCHF for this species were negative, and this is inconsistent with data obtained in the west of the country (Badji et al. 2023; Zeller et al. 1997). For example, an earlier study showed isolations of CCHFV from A. variegatum (Camicas et al. 1992) and its vectorial capacity was demonstrated (Faye, Fontenille, et al. 1999). Some authors claim that A. variegatum might play an important role in human infections; it is among the most important species that may have contact with humans (Mediannikov et al. 2010).

H. rufipes is the most widespread Hyalomma in Africa, ecologically related to H. truncatum, both species have been found in all bioclimatic zones studied. Their presence in the north (Sahelian zone) appears to be a re‐expansion of their distribution, as they were not collected by Gueye et al. (1987). Before the drought, however, these ticks usually infested cattle in this area. Both species show a strong preference for cattle and sheep, in which they mainly settle in the anogenital region and tail. H. rufipes is notorious as a vector of the CCHF virus (Camicas et al. 1994), it was found infected by CCHFV in two biogeographical areas in this study. Infected specimens were collected from cattle and goats with MIP of 2.1% and 1.2%, respectively. This species and H. truncatum have been designated as priority species to be monitored for CCHFV transmission (Camicas et al. 1986). CCHFV has been reliably demonstrated in unfed specimens of H. rufipes, and H. truncatum (Gargili et al. 2017), their vector competencies were proven (Faye, Cornet, et al. 1999) and a CCHFV infection rate of 18.6% was recently observed from H. rufipes in Mauritania (Schulz et al. 2021). The virological tests confirmed that Hylomma genus is the main vector of CCHF, and also showed the important role played by sheep and cattle in maintaining the virus, which has been demonstrated (Wilson et al. 1991). Our results are similar to those obtained in Senegal in a recent study (Badji et al. 2023) where only ticks collected from sheep and cattle were positive for CCHFV. Five of the six infected specimens were collected in the Sahelian zone, corroborating data obtained during an epidemiological investigation in this area, where the seroprevalence of CCHFV in animals was very high (Ngom et al. 2024). This area is a transhumance corridor between Senegal and Mauritania, one of the West African countries where the circulation of the virus is almost endemic (Nabeth et al. 2004).

The other species in this collection (R. geigyi, R. sulcatus, R. guilhoni, R. decoloratus, R. musahmae, R. lunulatus and H. impressum) are of little epidemiological importance, even if some have been found to be naturally infected with the virus (Camicas et al. 1986; Gargili et al. 2017).

5. Conclusion

This study updated some aspects of our knowledge (prevalence of tick infestation between hosts according to variables: gender, age, origin area; species composition, relative abundance, spatial distribution and attachment site preferences) on the livestock tick fauna of Senegal. The mean infestation rate (35.3%) varied by host species and bioclimatic area. The anogenital region was the main tick attachment site in the different hosts. Comparative analysis of tick infestation showed that age, gender and bioclimatic zone significantly affected tick infestation rates, but their impact varied according to host species. The most abundant of the 12 tick species collected in this study included R. evertsi (32.7%), H. impeltatum (20.1%), A. variegatum (10.7%), H. truncatum (10.0%) and H. rufipes (9.8%). Tick species composition and relative abundance varied by host species and bioclimatic area. Two species (H. impeltatum, H. rufipes) collected on sheep and cattle from Sahelian and Sudano‐Sahelian Zone belonging to the major vectors of CCHFV were found infected. The main limitation of our study is the low number of host species targeted and the single collecting method used. For a more exhaustive list of tick species in Senegal, it would be important to conduct a longitudinal study covering the 12 months of the year and combining different collection methods. Highly infested livestock and CCHFV‐positive ticks increase the risk of human infection. This study underlines the urgent need for a tick control strategy and close monitoring of CCHV. Animal serosurveillance will remain an essential tool for monitoring endemic transmission levels, and for investigating areas where CCHF virus circulation is unknown. It is very important to assess the potential role of domestic species in maintaining the virus.

Author Contributions

Aliou Khoule: investigation, validation, formal analysis, methodology, visualization, writing–original draft, writing–review and editing, data curation, software. Déthié Ngom: investigation, methodology, data curation, software, validation, formal analysis, writing–review and editing. Mouhamet Faye: investigation, methodology, writing–review and editing. Ousseynou Sene: investigation, methodology, validation, formal analysis, data curation, writing–review and editing. Aminata Badji: methodology, investigation, formal analysis, data curation, writing–review and editing. Elhadji Ndiaye: investigation, methodology, data curation, formal analysis, writing–review and editing. Gamou Fall: conceptualization, investigation, methodology, validation, formal analysis, funding acquisition, resources, writing–review and editing. Ibrahima Dia: investigation, methodology, formal analysis, validation, visualization, writing–review and editing. Mawlouth Diallo: investigation, methodology, validation, writing–review and editing, formal analysis, data curation. Diawo Diallo: conceptualization, investigation, funding acquisition, writing–original draft, writing–review and editing, visualization, validation, methodology, formal analysis, project administration, resources, supervision, data curation.

Ethics Statement

Livestock owners were orally informed by investigators about the objectives and the protocol of the study. After giving oral consent, the owners restrained and monitored the animals during tick collections. All ticks were collected by professional veterinarians and zoologists. After this collection, vitamins, antiparasitic and antibiotics were given to animals if necessary for the treatment of some infection. Tick sampling staff followed all biosafety measures to avoid the risk of tick‐borne infection and transmission from animals to humans. These biosafety measures included wearing protective clothing with long sleeves and pants, light‐coloured clothing to easily detect ticks; regularly checking for ticks on clothing and skin and carefully remove them if necessary; wearing latex gloves when handling ticks in the field; collecting ticks with tweezers; being careful not to crush them; placing ticks in sealed tubes, then store them in liquid nitrogen for transport to the lab. After collection sessions, all materials were cleaned and decontaminated. Staff, livestock owners and populations we also informed to avoid contact with biological fluids in animals, especially when giving birth, and to warm milk before use.

Consent

The authors have nothing to report.

Conflicts of Interest

The authors declare no conflicts of interest.

Peer Review

The peer review history for this article is available at https://publons.com/publon/10.1002/vms3.70165.

Funding: This research was funded by the National Institutes of Health (NIH/USA) (Grant number U01AI151758; Subaward #3‐IPD‐NIH‐U01‐AS‐2022).

Contributor Information

Aliou Khoule, Email: Aliou.khoule@pasteur.sn.

Diawo Diallo, Email: diawo.diallo@pasteur.sn.

Data Availability Statement

Data are available on request from the authors.

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