Ticks ( Acari : Ixodidae ) infesting camels ( Camelus dromedarius ) in Northern Sudan

ELGHALI, A. & HASSAN, S.M. 2009. Ticks (Acari: Ixodidae) infesting camels (Camelus dromedarius) in Northern Sudan. Onderstepoort Journal of Veterinary Research, 76:177–185 Monthly total body tick collections from 13-20 camels were conducted for 2 consecutive years (2000– 2001) in Northern Sudan. Tick populations were correlated with locality, season, predeliction site, sex and coat colour. Hyalomma dromedarii was found to be the predominant (89 %) tick species infesting the camels. Other tick species found in very low numbers were Hyalomma impeltatum (7.7 %), Hy alomma anatolicum anatolicum (3.3 %), Hyalomma truncatum (0.29 %), Hyalomma marginatum rufipes (0.25 %), Rhipicephalus praetextatus (0.30 %) and Rhipicephalus sanguineus group (0.09 %). Nymphs of the genus Hyalomma were collected in significant numbers. Adult ticks significantly preferred to attach to the lower parts of the camel’s body for feeding while the nymphs preferred the back of the animal. Female camels harboured more ticks than males while higher infestations were recorded on camels with a grey coat colour compared to those with a brown coat colour. Ticks were found on camels throughout the year and increased in numbers during March to October with a peak in September.


INTRODUCTION
Little publish information on ticks infesting camels is available.Camels in Egypt were found to be mainly infested by Hyalomma dromedarii (95 %) together with Hyalomma marginatum subspecies, Hyalomma anatolicum excavatum and Hyalomma species nymphs (Van Straten & Jongejan 1993).In the same area and on the same animal species Diab, El Kady & Shouky (2001) reported that H. dromedarii, Hy alomma impeltatum, H. a. excavatum and H. a. anatolicum represented 96 % of the tick population with a higher infestation in March to November and a mean monthly total of 22-78 ticks per animal.About 62 % of adult ticks were collected from the tail, anus, brisket and udder, and 91 % of nymphs were found infesting humps, neck, ears and sides.In Saudi Arabia, a total of 1 045 adult H. dromedarii and 174 H. a. excavatum together with 110 ticks that included H. a. anatolicum, H. impeltatum, Hyalomma schulzei, Hyalomma truncatum, Hyalomma mar gina tum rufipes and Hyalomma marginatum turanicum as well as 143 Hyalomma spp.nymphs were collected from 10 camels (El Khalifa, Al Asgah & Diab 1985).In Yemen, Arab Republic, the most abundant livestock ticks were Hyalomma spp., particularly on camels, but with a very low burden (MacAr tan, Hunter, Pegram & Bourne 1987).In the Sudan, Karrar, Kaiser & Hoogstraal (1963) reported that H. dromedarii was the main tick species of camels together with Amblyomma lepidum, H. impeltatum, Rhipi- cephalus sanguineus sanguineus, Rhipicephalus simus, H. a. excavatum, H. truncatum and H. m. ru fipes. Dolan, Wilson, Schwart, Newson & Field (1983) collected H. dromedarii, H. m. rufipes and Rhipicephalus pulchellus from camels in Kenya.The objective of this study was to conduct population studies of ticks infesting camels in Northern Sudan.

MATERIALS AND METHODS
The study area extends along the western banks of River Atbara starting from Ed Damer in Northern Su dan (Fig. 1).This area is in the arid (desert) zone (annual rainfall ranges between 0-100 mm) with very poor vegetation cover which mainly consists of scattered bushes and small trees, i.e.Prosopis chilen sis and Capparis decidua.Large acacias such as Acacia nilotica nilotica, Acacia seyal, Acacia tortilis tortilis, Acacia tortilis raddiana, Ziziphus spina christa and Hyphaena thebaica are abundant (El Amin 1989).Small-scale farms are cultivated along the river banks where camels graze.They graze on grass and post-harvest agricultural residues and browse on bushes and trees.During the wet seasons they move to the Butana area, approximately 300 km to the south-east, where the grazing is better.

Tick collection and identification
Total body collections of ticks from 13-20 adult camels were carried out on a monthly basis bar for 2 consecutive years (2000)(2001).Ticks from each predilection site were put into separate vials containing 70 % ethanol.The vials were labeled to indicate date, time, locality, animal number, sex, host coat colour and predilection site.The predilection sites included head (head and neck), back (hump region and flank), tail (tail shaft and perineum), lower parts (brisket, belly, udder or scrotum and inner sides of thigh) and feet (knee to pad).
The ratio of male to female ticks ranged between 3.1 ± 0.21 and 7.1 ± 1.2 for the 2 years, respectively.The total ratio of Hyalomma nymphs to adults of all Hyalomma species was 1:26.1.Female camels were found to carry more ticks than males.This result was highly significant for H. dromedarii (Table 4).
Hyalomma dromedarii numbers increased from April and reached a peak in September and October in 2000 (Table 5).In 2001, the highest infestation was recorded in March although there was no significant difference between months.Hyalomma impeltatum showed no significant differences between months in 2000 but the least mean tick numbers were collected in July and August.Peak numbers of this species were collected in March 2001 (Table 5) and the least in February, June and July.More H. a. anatolicum were collected in January 2000 and in November 2001 with no significant differences between months.Hyalomma nymphs were prevalent throughout 2000 and 2001 with peaks in November 2000 and July 2001 (Table 5).The total numbers of adult ticks collected were significantly higher in 2000 during September and October and from January to June but in 2001 there were no significant differences in the total numbers ticks collected per month.During the collection period, male ticks outnumbered females with the exception of H. a. anatolicum (Table 5).
Female camels with a grey coat colour harboured significantly more ticks than females with a brown coat colour (Table 7).This was shown clearly by individual tick species, their gender and also with mean total ticks collected.However, there were no significant differences in the numbers of nymphs harboured by grey and brown female camels.Male grey coloured camels harboured more ticks than brown coloured males but the difference was only significant for female H. dromedarii and for male H. a. anatolicum.
Hyalomma dromedarii infestation was positively correlated in 2000 with mean minimum and maximum ambient temperatures, relative humidity and rainfall (Table 8) while in 2001, this was positively correlated only with mean minimum and mean maximum ambient temperatures.Hyalomma impeltatum in 2000 and H. a. anatolicum in both years were found to increase with increased humidity and decreased temperature.Generally, tick infestation was not strongly correlated with meteorological values.It was, however, observed that Hyalomma nymphs significantly increased in number with rainfall during 2000.

DISCUSSION
This study was conducted in a semi-desert zone where rainfall is very low and of short duration (July to September).The River Atbara is a factor in that it creates suitable microhabitats for ticks with acacia trees, bushes, few grasses and cultivated areas and plays a role with the movement of camels to Butana from July to November in impacting on the seasonal population changes of ticks.
In the present study, H. dromedarii represented the main tick species infesting camels (88.9 %) followed by H. impeltatum (7.7 %) and H. a. anatolicum (3.3 %).It was also found that H. dromedarii females were the main tick species found engorged on the camels, while females of the other species (H.impeltatum, H. a. anatolicum, H. m. rufipes and Rhipicephalus spp.) were not engorged or only partially engorged.This could be due the fact that cam-els are not the preferred hosts of the latter tick species.
Other tick species found in this study in small numbers were H. truncatum, H. m. rufipes, R. sanguineus group and R. praetextatus.In Egypt, the main tick species infesting camels is H. dromedarii representing up to 95 % of ticks (Van Straten & Jongejan, 1993;Diab et al. 2001).In Eastern Sudan, Karrar et al. (1963) reported that H. dromedarii is the main tick species feeding on camels.Other tick species they found on camels were R. sanguineus, R. simus, H. a. excavatum and Amblyomma lepidum.In the current study, A. lepidum was not found despite the fact that some camels are taken each year to the Butana area where this tick species was previously found (Karrar et al. 1963).Ahmed (1999) studied tick infestations on sheep in the study area and found that 74 % of the ticks were H. a. anatolicum, 15 % R. sanguineus group, 2 % R. simus, 9 % Rhipicephalus evertsi evertsi and 0.5 % H. dromedarii.This strongly implies that sheep are not preferred hosts for H. dromedarii, while camels are not preferred hosts for H. a. anatolicum.He also reported that sheep were not infested with H. impeltatum, H. truncatum and H. m. rufipes.In the current study R. e. evertsi was not found feeding on the camels.These two studies in the same ecological zone where camels and sheep co-exist imply that there is a strong host preference of these ticks.
In this study most ticks were collected from the lower parts of the camels.Unlike other animal species (Hoogstraal 1956), the tail, despite the fact that it is short in camels, was found to be an important feeding site of ticks particularly the edges.This could be due the fact that the tail of camels has a less fat component or that due to the physiological status of camels in that the body temperature fluctuates during the day and that of the tail is possibly the least affected.The high percentage (64.5 %) of nymphs found on the back particularly the hump also differs from other animal species.This is could be due to the fact that the nymphs ( which attached as larvae) seek shelter within the hairy hump area and that it provides more humidity, or it may be that H. dromedarii nymphs prefer the back of their hosts.For instance, Hassan (1997) working on cattle, found that nymphs of Rhipicephalus appendiculatus and Amblyomma variegatum preferred the head region and the underside of the hosts, respectively.The high number of ticks collected from under the tail in this study is in agreement with the findings of Diab et al. (2001).Hylomma m. rufipes was found mainly under the tail particularly around the anus.The predi-lection site of this tick species is not different from that of cattle (Hoogstraal 1956;Hassan 1997).
Seasonality of ticks infesting camels was observed by Diab et al. (2001) who reported that high tick infestations in Egypt occurred during March to November.In the present study, there was no clear pattern of seasonality.Ticks were found on camels throughout the year but it was observed that the highest infestation occurred from March to October.This could be attributed to the fact that the non-parasitic flat stages could survive well during winter which was reflected as infestations during the following summer.On the other hand, it was observed that ticks do not go into diapause during winter when ambient temperature drops to about 10 °C.Hylomma a. anatolicum feeding on sheep in the same area were also not found to go into diapause, according to Ahmed (1999) who found high infestations in winter.It is also possible that H. dromedarii unlike R. appendiculatus (Pegram & Banda 1990) does not go into diapause.
This study revealed that female camels carried significantly more ticks than the males.This was true for all adult tick species.Hassan (1997) reported similar findings for cows with higher loads of R. appendiculatus and A. variegatum than oxen.Pregnancy and lactation stress may lower the resistance of females to tick infestation (Ali 2004).However, this was not true for nymphs as both genders of camels carried loads the differences of which were not significant.This could be due to differences in resistance of male and female camels against larvae that feed and moult on the host, but not against nymphs.
Camels with a grey coat colour carried significantly more ticks than those with a brown coat colour.This was true for all tick species particularly those which were found feeding on female camels.Working with cattle, Hassan (1997) found that hosts with a black coat colour were infested with fewer R. append iculatus and A. variegatum compared to cattle of a brown and white coat colour.He attributed this phenomenon to the fact that a dark coat colour absorbs more heat, changing the microhabitat of the ticks which leads to a high mortality rate or the ticks dropping off without feeding.Camels in this area are of two types, namely brown and grey, and the difference in tick load may indicate a difference in their innate resistance to tick infestation.
The current study revealed that male ticks of all species except H. a. anatolicum outnumbered females.Similar results were reported by Hoogstraal (1956), Kaiser, Sutherst, Bourne, Gorissen & Floyd (1988) and Hassan (1997).This is due to the fact that females detach from the hosts after a few days of feeding to oviposit while males remain for several weeks before dropping (Hoogstraal 1956).However, H. a. anatolicum females were found to outnumber males.This could be due to the fact that camels are probably not their preferred hosts and hence males either do not attach or drop off without attaching.Very few engorged H. a. anatolicum females were collected indicating that few males were available for mating with females to complete engorgement.
FIG. 1 Map of the study area in Nothern Sudan showing the localities from where ticks were colected (•) and Atbara Research Laboratory (■)

TABLE 1
Means (± SE) of ticks collected from camels along the River Atbara and Ed damer in 2000-

2001 Year Tick species River Atbara (123) Ed damer (62)
Ratio (nymphs:adults) 1:26.1 TABLE 3 Total numbers of tick species collected from camels in very low numbers during 2000 and 2001 in River Nile State, Northern Sudan TABLE 4 Means ( ± SE) of ticks collected from male and female camels in River Nile State, Northern Sudan, 2000-2001 Means ( ± SE) followed by the same letter in each row are not significantly different at 5 % level, based on Ryan's Q test (REGWQ) n = no. of animals used TABLE 5 Mean ( ± SE) numbers of ticks collected from camels in River Nile State in 2000 and 2001 Month Means (± SE) followed by the same letter in each row are not significantly different at 5% level, based on Ryan's Q test (REWGQ) No. of animals = 249

TABLE 7
Mean (± SE) number of ticks collected from male and female camels of different coat colour in River Nile State in 2000 and 2001