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. 2020 Oct 28;45(1):211–217. doi: 10.1007/s12639-020-01296-4

Identification and incidence of hard tick species during summer season 2019 in Jijel Province (northeastern Algeria)

Derradj Lotfi 1,✉, Kohil Karima 1,2
PMCID: PMC7921241  PMID: 33746406

Abstract

Ticks are haematophagous arthropodsand tick-borne diseases causes billions of dollars in losses in the cattle industry because of the ability of ticks to be vector for many pathogens. This paper identifies and compares the infestation rate (prevalence and intensity) of females of hard tick species compared to males with respect to sex, age and breed of cattle in the region of Jijel, northeastern Algeria. A total of infested 53 cattle were screened and 1214 ticks were collected manually during summer 2019 (June, July and August) and identified based on their morphology. Seven tick species were identified as infesting the cattle: viz. Rhipicephalus (Boophilus) annulatus, Rhipicephalus bursa, Rhipicephalus sanguineus, Hyalomma marginatum, Hyalomma lusitanicum, Hyalomma scupense, and Hyalomma anatolicum. The predominant tick species recorded is Rhipicephalus (Boophilus) annulatus. The maximum intensity of tick infestation as a function of age is between 3 and 4 years and 5 and 6 years (39 ticks/cow). The study shows that the comparison between the prevalence of infestation in females and males is significant as a function of sex and breed of cattle. In addition, only the intensity of infestation as a function of the age of the cattle, when comparing the sexes of the ticks, is significant (p < 0.05). This study also provides data for the development of an active control plan based on tick mating strategies for the management of ticks in cattle in Jijel, Algeria.

Keywords: Ixodes, Breton blackfoot, Plain redfoot, Brown atlas, Extensive system, Biotic factors

Introduction

In recent years, interest in ticks has increased. They feed on blood and serve as vectors for many diseases in vertebrates, especially mammals (Wall and Shearer 2008). Worldwide, over 700 species of hard ticks belong to 14 genera. Medical and veterinary importance genera are Ixodes, Dermacentor, Amblyomma, Haemaphysalis, Rhipicephalus and Hyalomma (Koc et al. 2015). Thus, losses due to tick infestation are enormous, for example in India, where it causes an annual loss of US$ 498.7 million (Minjauw and McLeod 2003); In Australia, Jonsson et al. (1998) reported that each engorging female Boophilus microplus tick was responsible for loss of 8.9 ml of daily milk production and 1.0 g body weight over a trial period of 15 weeks. Mediterranean theileriosis is widely distributed throughout southern Spain, where it causes economic losses of considerable importance (Viseras and Garcia-Fernandez 1999); in Algeria, losses in milk yield due to tick-borne diseases have been estimated at 319 L per cattle (Benchikh-Elfegoun et al. 2018).

For several years, a great effort has been devoted to studying the prevalence and intensity of tick infestations as a function of sex, age and breed of cattle; from Tunisia, United States, Saudi Arabia and Romania, respectively (M'ghirbi and Bouattour 2009; Williams-Newkirk et al. 2015; Alanazi et al. 2018, 2019; Domşa et al. 2016). These epidemiological indicators (prevalence, intensity) are fundamental for tick control programs because tick distribution has been controlled by biotic and abiotic factors (Stachurski et al. 1993; Boulkaboul 2003; Gharbi et al. 2013; Gharbi and Darghouth 2014).

In Algeria, Yousfi-Monod and Aeschlimann (1986) identified 12 species belonging to 6 genera in the western region and Boulkaboul (Boulkaboul 2003) identified 13 species and 6 genera in the province of Tiaret (South–West) without distinction of race, age or sex. In north-eastern Algeria (Jijel), Benchikh-Elfegoun et al. (2007) identified five species belonging to two genera (Rhipicephalus and Hyalomma), where cattle breeds have been grouped into two: Brown Atlas and Crossbreed, these cattle breeds are adapted to climatic conditions and there is an effect of age and breed of cattle on the infestation rate. Furthermore, Benchikh-Elfegoun et al. (2013) considered the first detailed study on biotic factors effect on ticks infestation, Benchikh-Elfegoun et al. (2018) provided a view about tick borne-diseases and milk yield losses; Benchikh-Elfegoun et al. (2019), in Constantine region, identified seven species belonging to four genera with a significate influence of cattle age on tick’s intensity. However, most of the previous studies do not take into account the prevalence of tick species, in particular the intensity, the infestation rate of female ticks relative to males in cattle, and the influence of biotic factors (cattle age, sex and breed).

This paper presents a new type of analysis of female tick infestation compared to male ticks. It is very important to study it to understand the relationship between biotic factors and tick mating, which can lead to its disruption during the high seasonal activity of some tick species. Thus, this work aims to determine, examine and compare the infestation rate of hard tick species infesting cattle and the correlation between female and male ticks regarding age, sex and breed of cattle in Jijel, Algeria, collected during summer 2019.

Materials and methods

Study area

This study was conducted in June, July and August 2019 in the province of Jijel in north-eastern Algeria (Fig. 1). Jijel is located between 36°48′N and 5°46′E, covers 2,577 km2. The region is dominated by a warm temperate climate with a typical hot and relatively dry season between June and August and a wet season from November to April. The annual precipitation varies between 800 and 900 mm/year, and the monthly temperature ranges between 11.3 and 26 °C. In Jijel, August and July are the hottest and driest months respectively (Source: climate-data.org).

Fig. 1.

Fig. 1

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The geographical location of Jijel Province, northeast Algeria

Sampling

The number of cattle herds in Jijel is estimated at 87,942 head (Hamiroune et al. 2019). There are 53 cattle including 7 males (13.20%) and 46 females (86.80%) chosen randomly from different farms, belonging to three breeds: Brown Atlas (35.85%), Breton Blackfoot (56.60%) and Plain Redfoot (7.55%). The different age groups selected for this study are less than one-year-old (5.66%), two years old (9.43%), three years old (13.21%), four years old (5.66%), five years old (9. 43%), six years (15.09%), seven years (13.21%), eight years (18.77%), nine years (3.77%) and less than eleven years (5.66%).

Cattle in the study area are bred according to an extensive system; they are kept on pasture 24 h a day and farmers only take cows to the barns for calving. Anti-tick control acaricides are applied randomly and inconsistently by farmers. For this study, ticks were manually removed from the surface of the skin of infested cattle. The ticks were visible in various parts of the cattle. They were collected without turning the tick, as the mouthparts would detach and remain in the skin. After removing the tick, we carefully clean the bite area and our hands with rubbing alcohol, iodine scrub or soap and water; 1214 ticks were collected and every ticks collected from each cattle were stored in vials containing 70% ethanol. Data on the age, breed and sex of the cattle were meticulously recorded, and the ticks were then identified under a stereomicroscope according to the key of Walker (2003) in the Laboratory of Biosystematics and Ecology of Arthropods.

Statistical analysis

All data were exported to an Excel® spreadsheet for Windows® to measure species frequency, infestation prevalence and intensity means for females, males in cattle, epidemiological indicators and sex ratio (Bush et al. 1997) as follows:

  • Infestation incidence (%) = 100 × (number of infested cattle/number of examined cattle)

  • Tick infestation intensity = the number of ticks/the number of infected cattle

  • Sex ratio = the number of females to the number of males (Martin and Hine 2015)

The Chi-square test (χ2) was carried out on the infestation rate of male and female ticks to assess whether there was a statistically significant difference in tick infestation (Wasihun and Doda 2013). The one-way analysis of variance (ANOVA) was used to compare the rate of tick infestation as a function of biotic factors (age, sex and breed of cattle) and significance (p value) was recorded at a level of 5% (p < 0.05; Debbarma et al. 2018).

Results

A total number of 1214 ticks were collected between June and August 2019 from cattle in the province of Jijel, north-eastern Algeria. These ticks were identified on the basis of their morphology; they belong to 2 genera, namely Rhipicephalus spp. (85.42%) and Hyalomma spp. (14.58%) and 7 species, vis. Rh. (Boophilus) annulatus (74.62%), Rh. bursa (10.46%), Rh. sanguineus (0.32%), Hy. anatolicum (1.56%), Hy. lusitanicum (4.11%), Hy. marginatum (5.51%) and Hy. scupense (3.37%) (Table 1). Overall, the results show that females outnumber males by a factor of three (Table 1). The number of females and males differs widely between each genus; in the genus Rhipiciephalus females outnumber males but the opposite is true for Hyalomma spp. In each species of Rhipiciephalus the number of females prevails and the number of males is higher in Hyalomma species (Table 1).

Table 1.

Adult ticks collected from cattle in Jijel, northeast Algeria

Species Ticks number (%)
Overall Females Males Sex ratio
Rhipicephalus 1037 (85.42) 891 146 6.1
Rh. (Boophilus) annulatus 906 (74.62) 821 (67.63) 85 (7) 9.65
Rh. bursa 127 (10.46) 67 (5.52) 60 (4.94) 1.11
Rh. sanguineus 4 (0.32) 3 (0.25) 1 (0.08) 3
Hyalomma 177 (14.58) 42 135 0.31
Hy. anatolicum 19 (1.56) 2 (0.16) 17 (1.4) 0.11
Hy. lusitanicum 50 (4.11) 19 (1.57) 31 (2.55) 0.61
Hy. marginatum 67 (5.51) 10 (0.82) 57 (4.7) 0.17
Hy. scupense 41 (3.37) 11 (0.9) 30 (2.47) 0.36
Total 1214 (100) 933 (76.85) 281 (23.14) 3.32
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Ticks cattle infestations based on sex, breed and age

The results show that the prevalence of female tick infestation in cattle breeds (99.49%) is statistically higher than that of male ticks (70.71%; p < 0.001). In addition, the prevalence of female tick infestation is significantly higher by sex of cattle (86.8%; 13.2%) compared to male ticks (p < 0.001). No statistically significant difference was found between the prevalence of infestation (p = 0.76) of female and male ticks and its intensity (p = 0.85) according to the age of the cattle (Table 2).

Table 2.

Adult ticks infestation rate according to cattle sex, age and breed in Jijel, northeast Algeria

Cattle Number Prevalence % Intensity (ticks/cow) Sex ratio
Age (years) Females Males Tick Females Males Tick
(0–1) 3 5.66 5.66 5.66 1.33 1.66 3 0.8
(1–2) 5 7.54 9.43 9.43 10.8 7.6 18.4 1.42
(2–3) 7 13.20 3.77 13.20 9 4.57 13.57 1.96
(3–4) 3 5.66 5.66 5.66 31.33 8 39.33 3.91
(4–5) 5 7.54 7.54 6.43 22.8 5.6 28.4 4.07
(5–6) 8 13.20 15.09 15.06 31.37 7.87 39.25 3.98
(6–7) 7 13.20 9.43 13.20 12.42 5.85 18.28 2.12
(7–8) 10 18.86 18.86 18.86 20.6 5.2 25.8 3.96
(8–9) 2 3.77 3.77 3.77 4 2 6 2
(10–11) 3 5.66 5.66 5.66 9 6.33 15.33 1.42
Sex
Female 46 93.47 89.13 86.8 19.19 7.14 24.7 3.49
Male 7 85.72 14.28 13.2 5.5 4 11.4 1.78
Breed
Brown Atlas 19 35.84 10.63 35.84 6 4.63 10.63 1.29
Red Pied Lowland 4 7.5 30.75 7.54 24.75 6 30.75 4.12
Breton Black Pied 30 56.6 29.33 56.6 22.96 6.66 29.63 3.44
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Furthermore, the results indicate that there is no statistically significant difference between the prevalence (p = 0.38) and intensity (p = 0.57) of tick infestation by cattle breed (Table 2). Similarly, the prevalence and intensity of tick infestation did not differ by cattle sex (p = 0.92; p = 0.96), respectively (Table 2). Moreover, there is no statistically significant difference in the prevalence of tick infestation (p = 0.09) by cattle age (Table 2). However, the results show that the infestation intensity is statistically significant (p = 0.006) (Table 3).

Table 3.

Adult ticks infestation rate collected from cattle in Jijel, northeast Algeria (total number of cattle examined = 53)

Species Cattle infested (prevalence %) Intensity (ticks/cow)
Females Males Species Species Females Males
Rhipicephalus
Rh. (Boophilus) annulatus 33 (62.26) 8 (15.09) 31 (58.49) 29 24.87 10.62
Rh. bursa 23 (43.39) 23(43.39) 25 (47.16) 5 2.91 2.6
Rh. sanguineus 1 (1.88) 1 (1.88) 1 (1.88) 4 3 1
Hyalomma
Hy. anatolicum 1 (1.88) 2 (3.77) 7(13.20) 2 2 8.5
Hy. lusitanicum 7 (13.2) 9 (16.98) 9 (16.98) 5 2.71 3.44
Hy. marginatum 6 (11.32) 11(20.75) 16 (30.18) 4 1.66 5.18
Hy. scupense 6 (11.32) 14 (26.41) 15(28.3) 2 1.83 2.14
Total 53 (100) 53 (100) 53 (100)
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Discussion

Overall tick infestations in cattle

Ticks are known to be of major medical and veterinary importance (Koc et al. 2015). Worldwide, the distribution of ticks is controlled by biotic factors such as age and sex of the hostand by abiotic factors such as temperature and humidity (Gharbi 2020). The distribution of ticks differs from one habitat to another (Ogden and Lindsay 2016). For example, Rh. (Boophilus) annulatus is known to be dominant in humid and sub-humid climates, Hialomma annatolicum in Africa extends from Ethiopia to North Africa where it occurs in Algeria, Libya and Egypt. It extends to north central Sudan, but does not appear to be well established south of the Sahara (Walker 2003). The current study describes tick infestation on cattle in Jijel region, Algeria. Out of 53 cattle, 1214 ticks were collected and identified during summer 2019 (June to August). Seven species of ticks were identified on the animals: Rhipicephalus (Boophilus) annulatus, Rhipicephalus bursa, Rhipicephalus sanguineus, Hyalomma marginatum, Hyalomma lusitanicum, Hyalomma scupense, Hyalomma anatolicum.

Rhipicephalus (Boophilus) sp. was found to be the predominant tick species in cattle, peaking in July with 29 ticks/cow. Effectively, this parasite is abundant in the Mediterranean, Palearctic and Afrotropical regions (Estrada-Peña et al. 2018) and Rhipicephalus (Boophilus) annulatus is a vector of Babesia bigemina, B. bovis and Anaplasma marginal (Walker 2003). In this study, Rh. annulatus were commonly found on cattle, particularly in the province of Jijel, peaking in July with 29 ticks/cow. This result is almost similar to previous studies carried out in other regions of Algeria of different climatic strata; Boutaleb (1982) in the sub-humid region (Constantine); Yousfi-Monod and Aeschliman (1986) in the Mediterranean region; Benchikh-Elfegoun et al. (2007) in the humid region; Rony et al. (2010) in the tropical region; Adrian (2012) in the arid region; Chhillar et al. (2014) in the semi-arid region; Kaur et al. (2015) and Debbarma et al. (2018) in the tropical and subtropical regions.. The results also indicate that the sex ratio is not significant; only in Rhipicephalus spp. the percentage of females is higher than that of males, while for Hyalomma spp. the percentage of males is higher than that of females (Gharbi et al. 2013). This can be explained by the fact that Hyalomma males are more mobile than females and stay longer on livestock. This result was also observed in dogs infested with the brown dog tick R. sanguineus (Little et al. 2007).

Biotic factors effect on prevalence and intensity of tick infestations on cattle

In this study, the prevalence of tick infestations in females was significantly higher than in males with respect to sex, age and breed of cattle. No significant differences in the prevalence and intensity of tick infestations related to sex, age and breed of cattle were found, which has also been reported previously (Ghosh et al. 2018; Abera et al. 2010). Age of animals plays a role in tick species infestation (Manan and Zabita Khan 2007), this may be explained by the fact that when cows get old, their immunity to ticks is getting stronger, in the other hand, due to the life style of animals because calves are generally raised in barns and do not pasture during the first months, so they are less infested than young cattle (Bouattour 2001; Manan and Zabita Khan 2007).However, the intensity of infestation by age category of cattle was found to be statistically significant in cattle with age mean of 3.5 and 5.5 years. Similar results were reported by Patel et al. (2013), Kaur et al. (2015), Debbarma et al. (2018), Ghosh et al. (2018) and Benchikh-Elfegoun et al. (2019).

Conclusion

Our results show that the rate of tick infestation varies according to biotic factors (sex, age and breed of cattle). The same applies to male and female ticks. However, further studies are needed in this area as well as in the other regions of Algeria. The data collection allows us to have a map of geolocation of ticks in Algeria and to establish an adequate control program.

Acknowledgements

Authors are highly thankful to the herdsmen for their permission to collect ticks from their cattle. We gratefully thank Dr Subhamoy Ghosh (Central Agricultural University, Selesih, Aizawl, India) for editing the English.

Author contributions

All authors participated in the study design. DL collected ticks and conceived the manuscript, KK planned the research and identified tick species.

Funding

The current research received a grant from Arthropods Biosystematics and Ecology laboratory, Frères Mentouri – Constantine 1 University, Constantine, Algeria.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Footnotes

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Contributor Information

Derradj Lotfi, Email: lotfi.derradje@umc.edu.dz.

Kohil Karima, Email: kohil-8@hotmail.com.

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