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Difference in tick infestations: Hyalomma dromedarii and Rhipicephalus sanguineus sensu lato in southern Algeria

The aim of this study was to identify the species and parasitic indices of ticks. A flock of 57 individuals (sheep, goats, cattle and dogs) in southern Algeria was studied from March 2019 to February 2020 during monthly visits. A total of 2544 ticks were collected by examining the entire body of the animal. Two tick species were identified: Hyalomma dromedarii (2430 ticks) and Rhipicephalus sanguineus sensu lato (114 ticks). The first species had annual activity and consisted only of adults, while the second species had spring and summer activity and contained both adults and nymphs. At the annual level, the prevalence of infestation, abundance, and intensity were 38.60%, 44.63 and 115.64 ticks per animal, respectively. At the monthly level there were species specific fluctuations, with a peak in activity in September.


Introduction
Ticks (order: Ixodida) are blood-sucking ectoparasites considered to be among the most important vectors in the phylum Arthropoda (Goddard, 2012). They can transmit a large number of pathogens to domestic and wild animals and even to humans, e.g. bacteria such as Borrelia, Rickettsia, Bartonella, Coxiella, Ehrlichia, Anaplasma (Dantas-Torres et al., 2012), viruses such as meningoencephalitis virus, haemorrhagic fever virus (Moutailler et al., 2016) and parasites such as Babesia and Theileria (Martinot et al., 2011).
These pathogens present a real danger to animals and humans, and are responsible for emerging and/or re-emerging diseases worldwide (De la Fuente et al., 2017), particularly in tropical regions (Jongejan and Uilenberg, 2004). In fact, ticks are considered a major obstacle in improving breeding and they cause significant economic loss (Walker et al., 2003).
In Algeria, few studies have addressed the pathogenic role, biodiversity and dynamics of tick populations (Boulkaboul, 2003). In this sense, such studies are rare in the arid regions of Algeria. Therefore, the aim of the present study was to identify ticks in domestic animals in southern Algeria, in order to better manage and control these pathogens. A second aim was to determine the prevalence, abundance and intensity of annual and monthly tick infestations.

Study area
The study was carried out in Sidi Makhlouf in the Laghouat region (southern Algeria, N34°7′60″ E3°1′0″), which occupies an area of 142,000 hectares at an altitude of 900 m. It is located about 40 km north of the city of Laghouat, bounded to the north by the commune of Ain bel, to the east by the commune of Messaad, to the west by the commune of Douais and to the south by the commune of Laghouat (CDF, 2018).

Animals included in the study
A total of 57 animals were studied during the study period. All the animals were kept in semi-intensive farming systems without acaricide treatment (Table 1).

Collection, conservation and identification of ticks
Tick collection was carried out monthly over the course of one year; from March 2019 to February 2020. After the animal was restrained, the entire body was examined for ticks, which were gently removed by hand ensuring preservation of the tick body integrity, especially the gnathosoma which plays a very important role in tick species identification (Abdul Hussain et al., 2004). Ticks were then kept in labelled bottles (number, species, sex, date of collection) containing 80% ethanol, 15% water, 5% glycerol and 1% chloroform (Walker et al., 2003). At the laboratory, ticks were identified using a stereoscopic microscope (ZEISS SteREO Discovery. V8), according to the morphological keys (Estrada-Peña et al., 2017).

Statistical analysis
The following annual and monthly epidemiological indices were calculated (Bush et al., 1997):

Results and discussion
During the study period, a total of 2544 ticks were collected. The number of collected ticks was variable from month to month. The greatest tick activity was recorded in September, with a percentage of 18.95%, while the lowest was in March

Epidemiological indices
During the study period, the annual prevalence of infestation was 38.60%, abundance 44.63 and intensity 115.64 ticks per animal. The data for the monthly level and by animal species are shown in Table 2.
Sheep were only infested in August, when the prevalence, abundance and monthly intensity were 20%, 0.75 and 3.75 ticks per animal respectively. No infestation was observed throughout the study period in goats. This may be due to the immunity of these hosts (Boulkaboul, 2003), or the biotic (climate and environment) and abiotic (age, sex, race and immunity) factors that influence tick infestation prevalence (Dantas- Cattle were infested year round, with a prevalence ranging from 7.14 to 100%, abundance between 0.21 and 43.82 and intensity between 3 and 46.50 ticks per animal. Both tick species were collected, with a predominance of Hyalomma dromedarii; a species with annual activity, which is widespread in arid, desert and Saharan bioclimatic zones (Bouattour, 2002). A study carried out by Abdul Dogs were tick-free between September and January, while both tick species were found on dogs in all remaining months, with a predominance of Rhipicephalus sanguineus sl. The prevalence was between 25 and 100%, abundance between 0.25 and 13.5 and intensity between 1 and 13.5 ticks per animal. In another study (Matallah et al., 2013) found Rhipicepalus sanguineus

Distribution of Hyalomma dromedarii
The monthly evolution of adult females and males of Hyalomma dromedarii (March 2019-February 2020) in the Sidi Makhlouf area ( Figure 5) showed that adult males were more numerous than females (63.46% males, 36.54% females). This difference was due to the behaviour of male ticks. They can mate several times, and stay on the host for longer, while females mate only once and die after oviposition (Sonenshine et al., 1989;Walker et al., 2003;Latif and Walker 2004). The absence of nymphs and larvae is due to their feeding behaviour, i.e. they generally feed on small to medium-sized hosts, while adults feed on larger animals (Stafford, 2007). The hosts of Hyalomma dromedarii preimagos (nymphs and larves) are mainly rodents, rabbits and birds (Apanaskevich et al., 2008).
In similar studies, this species has been reported on dromedaries in the Adrar region, southern Algeria (Bouhous et al., 2008), and in camels and dogs in Riyadh, Saudi Arabia (Chandra et al.,  2019).
In a similar follow-up studies some authors have shown the presence of this species in dromedaries in the Adrar region, southern Algeria, (Bouhous et al., 2008) and in camels and dogs in Riyadh, Saudi Arabia (Chandra et al., 2019).
In the current study, this species was found on cattle and sheep. Figure  6 shows some of the fixation sites in cattle, generally by udders and testicles, sometimes the baleen, the anus margins, the feet, and the belly. Arches and belly were the fixation sites in sheep.

Conclusions
This study was carried out to determine the different species of ticks found on farm animals in the Sidi Makhlouf area, and to determine the monthly and annual epidemiological indices. The study showed that cattle were the most infested animals, followed by dogs and sheep, while goats were tickfree. During the study period, two tick species were collected and identified: Hyalomma dromedarii (95.52%) and Rhipicephalus sanguineus s.l. (4.48%). The first species had an annual activity while the second had a spring and summer activity.
In view of these results, future surveys should focus on the identification of ticks in different areas and on other animals. In particular, sheep and goats that showed little or no tick infestation in this study.  Ključne riječi: krpelj, Hyalomma dromedarii, Rhipicephalus sanguineus sensu lato, infestacija