Abstract: Background and Objectives: Ticks are the major vectors of different pathogens to humans and animals. The aim of this study was to determine the current status of tick species infesting domestic and wild animals and their seasonal population dynamics. Materials and Methods: This survey on tick species composition was carried out in Riyadh province, Saudi Arabia between January and December, 2017. Ticks were collected from the bodies of 18 domestic and wild animals. A total of 11,587 ixodid ticks (6,247 females; 4,585 males; 755 nymphs) were collected and preserved in 70% alcohol and then identified as to species. Results: The identified specimens belonged to ten species, including two genera of Hyalomma and Rhipicephalus. In domestic animals, the Hyalomma species comprised 68.3% and Rhipicephalus species 31.7%. Hyalomma dromedarii (39.9%) was the most common and abundant species, followed by Rhipicephalus turanicus (34.9%), while Rhipicephalus sanguineus was the most common species in wild hosts (83.0%). In addition, tick populations were most prevalent during summer and spring (36.0 and 31.6%, respectively). Conclusion: The results of this study showed that some tick species have expanded their distribution elsewhere to their previously recognised locations in Saudi Arabia. Moreover, the results of this study provide new data that government authorities can implement to take prevention measures for diseases transmitted by ticks.
INTRODUCTION
Ticks are globally significant vectors of an array of viral, bacterial and protozoal pathogens resulting in a wide range of animal diseases1. In some cases, tick-borne pathogens are zoonotic and a direct threat to human health. Other effects of tick feeding include: anaemia, paralysis, immunosuppression and invasion of tick bite wounds by secondary bacterial pathogens. Hence, through the combined direct and indirect deleterious effects, ticks and tick-borne disease pose a major threat to the health and welfare of domestic livestock and food security2.
In Saudi Arabia, the agriculture and livestock sector contributed 2.7% to the country’s gross domestic product (GDP)3 and the livestock populations are estimated at more than 27 million heads. Furthermore, thousands of livestock are imported annually from neighbouring countries such as Sudan, the Arabian Gulf countries and others such as Turkey, Argentina, Pakistan, Australia and Uruguay4. Camel, sheep, goat and cattle production plays an integral part in the agricultural sector and culture and contribute significantly to the food security of the country. On top of this, Saudi Arabia has one of the most species-diverse wild mammal populations in the Middle East, including the Arabian wolf, red fox, rock hyrax and various species of rodent that also play roles in the ecosystem of Saudi Arabia5.
Previous studies have recorded 15 ixodid species and subspecies infesting domestic and wild animals in different regions of Saudi Arabia6-14. However, there is no data available more recently than 2007 on the tick’s prevalence and distribution in Riyadh province. Therefore, the objective of this study was to determine the current status of tick species infesting domestic and wild animal hosts from that province.
MATERIALS AND METHODS
Study areas: The investigation was conducted between January and December, 2017 in the Riyadh province of Saudi Arabia,which has an area of 404,240 km2 and is located in the central part of Saudi Arabia between 24°38'N and 46°43'E. The region is divided into 19 governorates (Fig. 1).
| Fig. 1: | Location of the study area in Saudi Arabia |
The province has one of the largest livestock populations in Saudi Arabia, accounting for 20% of the country’s camels, 33% of its cattle, 17% of its sheep and 14% of its goats4. Additionally, the province has one of the most diverse populations of wild mammals, including species such as the Arabian wolf, red fox, rock hyrax and various rodents5,15.
Climatological data: The seasons were defined as follows: Summer: June, July and August; Autumn: September; October and November; Winter: December, January and February and Spring: March, April and May. Mean monthly minimum and maximum temperatures, mean rainfall and relative humidity for the Riyadh region was obtained from the Presidency of Meteorology and Environment (PME), available at https://www.pme.gov.sa. Riyadh province has a very hot summer with temperatures often approaching 50°C. The average high temperature in July is 45°C. Winters are cold with windy nights. The overall climate is arid, receiving very little rainfall (around 21.4 mm as an average) and with relative humidity ranging from 10-47% throughout the year. The region is also known to have many dust storms.
Study design: Ticks from camels, cattle, sheep, goats, horses, donkeys, rabbits were collected monthly from different locations in Riyadh province between January and December, 2017. The sample sizes varied at each visit: samples from sheep and goats numbered between 60 and 155 per visit, camels 20-60 and10-15 horses and donkeys10-15, on average (Table 1). Ticks from the Arabian wolf and red fox were obtained from hunters who collected them during the winter season. Meanwhile, rock hyrax, dogs, cats and rodents were trapped in the summer and winter seasons using live bait straps and examined in situ for tick infestations (Table 1).
Ticks collection and morphological identification: Ticks were collected from each animal and placed into 24100 mm vials containing 70% alcohol. Each vial was labeled and sent to the Parasitological Laboratory at Shaqra University, Saudi Arabia, as well as to the Parasitological Laboratory at Plymouth University, UK. Ticks were identified under a stereo microscope according to their morphological characteristics. This was done using taxonomic keys1,16,17.
Statistical analysis: All data was processed using SPSS version 18 software. The differences in parasite prevalence between different groups, ages, sexes and localities were analysed using the Chi-square test and the mean values were considered significantly different when p<0.05.
RESULTS
In this study, 5522 out of 8435domestics and wild animal hosts (65.5%) were found to be infested with ixodid ticks. A total of 11587 tick specimens (6247 females, 4585 males and 755 nymphs) were collected from 7944 domestic animals and 491 from wild animals (Table 1).
| Table 1: | Total numbers of animals and prevalence of ticks found in Riyadh province (January-December, 2017) |
| Table 2: | Numbers and prevalence of ticks collected from domestic animals in Riyadh province January-December, 2017 |
All the ticks belonged to the family Ixodidae. The identified tick specimens belonged to ten species, including two genera of Hyalomma and Rhipicephalus. Psammomys obesus and camels were the most tick-infested animals with prevalences of 100 and 85.20% respectively, while infestation of ticks in cats and rabbits was far less prevalent at 13 and 26.50% (Table 1). Hyalomma dromedarii (n = 3916, 34.43%) was the most common and abundant tick species, followed by Rhipicephalus turanicus (n = 3064, 27.30%), while Hyalomma schulzei was found only in camels with a prevalence of 0.40% (Table 2). In wild hosts, Rhipicephalus sanguineus was the most common species (n = 313, 83.0%) (Table 3). In the current study, tick populations were more prevalent during summer and spring with incidences of 4171(36.0%) and 3665 (31.6%), respectively (Table 4). Animals of both genders were infected with ticks, at different percentages (Table 5).
DISCUSSION
Overall, a tick infestation rate of 65.5% is in general agreement with previous studies from Saudi Arabia1,8-10,12,18,19. Ticks belonging to genus Hyalomma are dominant in the present study and found to be the most diverse group. Hyalomma dromedarii is wide spread in North Africa, Middle Eastern countries and Central and South Asia1. This study is in agreement with previous studies which indicated that this species is the most abundant tick in Saudi Arabia and is found in all are as investigated8,10,20,21. Generally Hy. dromedarii infests camels but can also infest cattle, sheep, goats, horses, donkeys and mules22. Many other animals can also be occasional hosts, including dogs, rodents and other wild animals23,24. H. impeltatum, H. anatolicum, H. excavatum and H. turanicum infestations in Saudi Arabia were most frequently found infesting camels, cattle, sheep and horses9,10,12,20, though the composition of tick species differ elsewhere, especially in regions geographically far from Saudi Arabia such as Europe, Brazil and South and Central Africa. For example, Grech-Angelini et al.25 surveyed ticks on cattle, small ruminants, domestic carnivores and wild animals on the French Mediterranean island of Corsica. Rhipicephalus bursa was found to be the main tick species infesting cattle, goats and sheep in this area, while H. marginatum was the main tick species on horses. Low numbers of other tick species were found on cattle and small ruminants, such as H. marginatum, H. scupense, I. ricinus, H. punctata, R. sanguineus, R. (Boophilus) annulatus and D. marginatus. The findings also reported that Rh. sanguineus was the main tick species on dogs and cats, though a small number of H. marginatum and I. ricinus ticks were found on those animals also. It was noticed that the tick D. marginatus was the main tick species found on wild boars on Corsica, while R. bursa was the main tick species on mouflons. Only I. ricinus was found on deer. In Brazil, Acosta et al.26 found the following seven tick species for the first time in Espírito Santo: Amblyomma aureolatum, Amblyomma coelebs, Amblyomma ovale, Amblyomma rotundatum, Amblyomma varium, Haemaphysalis juxtakochi and Ornithodoros hasei. They also reported that despite being previously recorded there, the species A. longirostre seemed to have disappeared. Horak et al.27 determined the species composition of ticks infesting inewhite and black rhinoceroses in southern Africa. Nineteen tick species were recovered, of which two Amblyomma rhinocerotis and Dermacentor rhinocerinus are known to prefer rhinos as hosts. Turner et al. 28 collected twelve ixodid tick species from mammals, birds and reptiles in central and northern Namibia, as follows: Amblyomma exornatum from lizards, Amblyomma latum from snakes, Amblyomma marmoreum from reptiles, H. rufipes and H. truncatum from domestic and wild ungulates, Rhipicentor bicornis from wild and domestic carnivores, Rhipicentor nuttalli from hedgehogs, porcupines, leopards, other wild carnivores and domestic dogs, R. gertrudae from larger herbivores, R. sulcatus from black-backed jackals and plains zebras, R. theileri from yellow mongooses, meercats and cape ground squirrels and finally R. turanicus which was collected from wild hosts including several large carnivores, hares and various ground-feeding birds.
| Table 3: | Numbers and prevalence of ticks collected from wild animals in Riyadh province (January-December, 2017) |
This study is the first to report H. schulzei in camels in the Riyadh province. This tick is the most abundant to parasitize camels in the arid northern frontier region of Saudi Arabia12 and has been reported in Southern Iraq near the Saudi Northern frontier border29 as well as in other neighbouring countries such as Iran30,31. The occurrence of H. Schulzei in camels from the Riyadh province may be attributed to camel movements, as they travel through deserts, villages and towns and could acquire many different ticks during their journeys.
The only tick to be recovered from all wild hosts in this study, with the exception of the Arabian wolf, was H. impeltatum from genus Hyalomma, a species which is found in western, eastern and Northern Africa, as well as the Middle East. In Saudi Arabia, juvenile stages have been found on Acomysdimidiatus, Merioneslybicus and Merionesrex, Psammomy sobesus and Paraechinus aethopicus13,14,19. Hyalomma spp. are well known vectors of numerous human and animal pathogens across Africa, Europe and Asia and they are of significant veterinary and medical importance due to their role in the transmission of pathogenic microorganisms32. In Saudi Arabia, both Sindbis and Dhori viruses (causing human febrile illnesses) have been identified in H. Impeltatum33. This tick has also been confirmed as a vector of Crimean-Congo Haemorrhagic Fever Virus34 of which there was an outbreak in 1990 involving seven individuals in the west of Saudi Arabia35. In addition it has also been implicated in the fatal transmission of Theleriahirci to sheep in Saudi Arabia36. Hyalomma anatolicum could be the vector of Theleriaovis and Theleriahirci in Saudi Arabia’s sheep37. Furthermore, Hyalomma spp may be a possible vector of Babesiacaballi and Theleriaequi in Saudi horses38,39.
This study found that Rhipicephalus ticks comprise four species, which is in agreement with findings of Diab et al.21, Al-Khalifa et al.19 and Asiry and Fetoh14, who reported R. sanguineus, R. turanicus, R. evertsievertsi and R. camicasi on both domestic and wild animals in Saudi Arabia. R. turanicus is widespread among domestic animals. In a nationwide survey, Diab et al.10 found R. turanicus to be the tick species which most often infests sheep and goats, with prevalences of 41.2 and 55.6%, respectively. This species was also reported in cattle and camels10. This species is being reported for the first time in hedgehogs in Saudi Arabia, although Youssefi et al.40 previously found this tick in hedgehogs in Iran. In Saudi Arabia, previous studies have recorded R. sanguineus and juvenile stages of H. impeltatum in hedgehogs13, which are animals that are widely distributed in Saudi Arabia and are already identified as hosts for a wide variety of zoonotic pathogens41.
| Table 4: | Numbers and the prevalence of ticks in different seasons collected from domestic and wild hosts in Riyadh province (January-December, 2017) |
| Table 5: | Tick preferences by gender of animal species in Riyadh province (January-December 2017) |
Rhipicephalus sanguineus was reported previously in Saudi Arabia in rodents and wild animals13,14,19,42, with the Arabian wolf and red fox showing 50% infestation rates. This is not surprising since their diet includes mammals, reptiles and birds, which constitute potential hosts for immature stages of ticks43,44.
Rhipicephalus evertsievertsi was reported previously in small ruminants from western and south western provinces of Saudi Arabia11,35. This tick has been described as preferring hosts such as horses, mules and donkeys17 and having the capability to tolerate a broad diversity of climatic conditions45. Rhipicephalus camicasi has rarely been reported in Saudi animals compared with other Rhipicephalus groups. In previous studies R. camicasi was observed in two native sheep in the western province of Saudi Arabia35 and Harrison et al.13 reported this species infesting Acomysdimidiatus at the National Wildlife Research Centre (NWRC) in Taif, in the west of the country. In addition, Abdel-Shafy46 found R. camicasi on camels in Egypt. Species belonging to genus Rhipicephalus are vectors of a wide range of pathogens diseases such as bebesia, the leria, rickettsia and Q fever17, which affect both humans and livestock in Saudi Arabia.
The frequency of ticks encountered during this study varied from season to season and was found to be highest in spring and summer, which is in agreement with previous studies47,48. Ticks are highly susceptible to climate change, largely as a result of the duration of their off-host life-cycle stages. Life-cycle processes such as development and survival are highly temperature- and moisture-dependent49. Depending on the relative effects of temperature on development and mortality at different stages of development, the outcome in terms of abundance are likely to vary, especially when seasonality is taken into account50. For most vectors, the greatest effect of climate change on transmission is likely to be observed at the extremes of the range of temperatures at which transmission occurs51,52. Therefore, Saudi Arabia’s environment is suitable for the rapid development of various tick species due to its wide range of climatic conditions.
CONCLUSION
Numerous tick species are spread throughout the Riyadh province and these include those of veterinary and economic significance. Several of the vector tick species have expanded their area of coverage outside that which has been previously recorded; this may lead to the expansion of tick-borne diseases to new areas, where outbreaks of disease are expected to be radical. Further epidemiological research should be carried out in the country to monitor the distribution of tick species and suggest effective control strategies.
SIGNIFICANCE STATEMENT
This is the first study recording the infestation of wild animals by various tick species in the Riyadh province and the first to report Hy. Schulzei and Rh. evertsievertsi in domestic animals there, though they have previously been recorded in other areas. This study will help researchers and government authorities in Saudi Arabia to develop their understanding and application of control strategies that can best prevent humans and animals from tick infestations.
ACKNOWLEDGMENTS
We thank the staff members of the Biological Science Department, Faculty of Science and Humanities at Shaqra University and the staff members of the School of Biological Science at University of Plymouth, UK for their technical support.