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Veterinary Parasitology 177 (2011) 353–358

Contents lists available at ScienceDirect

Veterinary Parasitology

journa l homepage: www.e lsev ier .com/ locate /vetpar

ife cycle of Hyalomma anatolicum Koch, 1844 (Acari: Ixodidae) fed onabbits, sheep and goats

.M. Ahmeda, K.M. Tahab, A.M. El Husseinc,∗

Department of Biology, Faculty of Education, Nile Valley University, Atbara, SudanVet. Res. Laboratory, Atbara, SudanCentral Laboratory, Ministry of Sci. and Tech., P.O. Box 8067, Alamarat, Khartoum, Sudan

r t i c l e i n f o

rticle history:eceived 9 June 2010eceived in revised form 6 December 2010ccepted 13 December 2010

eywords:yalomma anatolicumife cycleabbits

a b s t r a c t

Some aspects of the biology of the tick Hyalomma anatolicum fed on rabbits, sheep andgoats were studied. The non-feeding stages were maintained under laboratory conditions at20–36 ◦C and 75% relative humidity. The longest feeding periods of larvae and nymphs of H.anatolicum were observed when fed on rabbits (mean 4.58 ± 0.51 and 7 ± 1.15 days, respec-tively) while the longest feeding periods of females were observed on goats (9.61 ± 1.21).The pre-oviposition period (4.8 ± 0.42 days) and pre-eclosion periods (mean 21.3 ± 1.16days) were shortest for females fed on rabbits. Engorged females reached heavier engorge-ment weights (482.92 ± 88.08 mg), and produced more eggs (4881.8 ± 842.71) when fed

heepoats

on rabbits. However, no significant differences were observed between the percentageshatchability of eggs laid by ticks fed on the three hosts studied.

Most (94.31%) of the larvae fed on rabbits underwent a 2-host life cycle, while few (5.69%)of them behaved as a 3-host ticks. Few larvae were able to complete feeding as 3-hostpattern on both sheep and goats, while the majority of the larvae failed to complete feedingor died on their way to molt on both sheep and goats.

© 2010 Elsevier B.V. All rights reserved.

. Introduction

Types of hosts have pronounced effect on viabil-ty and fecundity of feeding ticks. Dipeolu and Adeyefa1984) showed that ticks (Hyalomma rufipes (Koch) Ambly-mma variegatum (Fabricius), Rhipicephalus (Boophilus)ecoloratus (Koch) and Rhipicephalus (Boophilus) geigyiAeschliman et Morel)), detached from sheep and horsesaid significantly fewer eggs and were biologically less

iable than those fed on cattle. They concluded that theatter are better hosts. Dipeolu and Akinboade (1984) com-ared fecundity of A. variegatum and R. (B) decoloratus fedn the red flanked duiker and cattle. Ticks fed on duiker pro-

∗ Corresponding author.E-mail address: abdelhussein@hotmail.com (A.M.E. Hussein).

304-4017/$ – see front matter © 2010 Elsevier B.V. All rights reserved.oi:10.1016/j.vetpar.2010.12.012

duced more eggs even though their engorgement weightswere similar to those fed on cattle.

Hyalomma anatolicum, previously known as H. ana-tolicum anatolicum, has been re-described and named byApanaskevic and Horak (2005). It is one of the mosteconomically important ticks in the Sudan. Both tropi-cal theileriosis of cattle due to Theileria annulata infectionand malignant theileriosis of sheep due to Theileria lesto-quardi are mainly transmitted by H. anatolicum in thiscountry (Anon., 1983; El Hussein et al., 2005; Salih et al.,2005).

Recent reports from field studies in Africa indicated

that acaricide treatments alone did not decrease the num-bers of ticks satisfactorily. Integrated control methods arenow being strongly advocated, this in turn necessitatesthat detailed information on biology and ecology of eco-nomically important tick species such as H. anatolicum be

354 B.M. Ahmed et al. / Veterinary Parasitology 177 (2011) 353–358

Table 1Feeding behavior of Hyalomma anatolicum larvae fed on rabbits, sheep and goats.

Host Replicates No. of larvaeapplied peranimal (total)

% of engorged larvae detachedas 3-host cycle (mean ± SD)

% of engorged nymphsdetached as 2-host cycle(mean ± SD)

Rabbits 2 150 (300) 5.69 ± 1.00 94.31 ± 4.48

The feeding periods of nymphs ranged between 6 and 8days (mean 7 ± 1.15) when fed on rabbits. These were sig-nificantly longer (P < 0.001) than those recorded on sheep

Table 2Feeding behavior of Hyalomma anatolicum nymphs detached as 2-hostcycle when fed on rabbits.

Days from initial contact No. of nymphsdetached

15 171 (85.93)16 14 (7.03)17 5 (2.51)18 1 (0.50)19 2 (1.01)20 2 (1.01)

Sheep 2 150 (300)Goats 2 300 (600)

gathered to help formulate successful control programs(de Castro, 1997; Willadsen, 2006).

The present series of experiments were thus designedto investigate the life cycle and the biotic potential of thetick H. anatolicum on three hosts viz; rabbits, sheep andgoats. These hosts are usually raised in mixed flocks inRiver Nile State/Sudan where the present study was con-ducted. Malignant ovine theileriosis is considered as one ofthe major diseases of sheep in this area (El Hussein et al.,1993; El Ghali and El Hussein, 1995; Ahmed et al., 2003).While local goats can be infected without manifesting clin-ical signs or untoward effects (Taha, 2000).

2. Materials and methods

The original laboratory colony of the tick H. anatolicumwas established from two engorged female ticks collectedfrom sheep at El-Akad area, River Nile State (300 km Northof Khartoum at River Nile bank).

Desert sheep (Ovis aries) (4–5 months old), Nubian goats(Capra hircus) (5–7 months old) and adult local rabbitsobtained from local market were used to feed the differentstages of ticks. The flat larvae, nymphs and adult ticks wereapplied to ears of rabbits, sheep and goats using ear bagsaccording to Bailey (1960). Nymphal stage ticks for feedingon sheep and goats were obtained from larvae fed on rab-bits. Two animals of each host species were used to feedeach of the three stages of the ticks. Ticks were observed atleast for three weeks and the feeding periods, the numbersof engorged larvae, nymphs and female adult ticks wererecorded.

The engorged stages of ticks (engorged larvae andengorged nymphs) were kept at room temperature(20–36 ◦C), and 75% relative humidity using specimentubes, desiccators and saturated solutions of sodium chlo-ride (Winston and Bates, 1960). Daily maximum andminimum temperature were recorded using thermometersplaced inside the desiccators. Engorged female ticks fromeach rabbit, sheep and goats were individually weighedon the day of detachment. They were placed in specimentubes and maintained under the conditions mentionedabove. The pre-eclosion periods were recorded and thenumbers of eggs for each female tick were estimated.

Hatchability of eggs laid by various females were recordedand expressed as percentages. Data recovered from theabove studies were analyzed using t-test, linear regres-sion and correlation using both scientific calculator andcomputer.

6.33 ± 6.12 024.33 ± 5.18 0

3. Results

3.1. Feeding and molting of larvae

Hungry larvae attached readily within 24 h after beingreleased on rabbits, sheep or goats. As shown in Table 1larvae fed for 4–5 days (mean 4.58 ± 0.51) on rabbits whichwas significantly (P < 0.001) longer than those fed for 4–5days (mean 4.05 ± 0.23) and 2–5 days (mean 3.13 ± 0.55)on sheep and goats, respectively.

Table 1 shows that the numbers of engorged larvaedetached from sheep and goats were few, being only 6.33%and 24.33%, respectively. On all of the groups of sheep orgoats, larvae that were likely to undergo 2-host life cyclefailed to complete molting on these hosts (Table 1). In con-trast, most of the larvae fed on rabbits (94.31%) underwent2-host life cycle and started to drop as engorged nymphson day 15 post initial contact and continued to drop upto 23 days post the initial contact (mean 15.37 days)(Table 2). Few of the larvae (5.69%) behaved as a 3-host tick(Table 1).

Engorged larvae detached from rabbits molted within17–18 days (mean 17.2 ± 0.45) and those detached fromsheep molted within 16–18 days (mean 17.05 ± 0.71).These were significantly (P < 0.001) longer than thosedetached from goats that molted within 9–12 days (mean10.5 ± 2.12) (Table 3).

3.2. Feeding and molting of nymphs

21 2 (1.01)23 2 (1.01)

Total 199 (94.31)

Numbers between parentheses represent percentages from the total num-bers of nymphs detached from rabbits.

B.M. Ahmed et al. / Veterinary Parasitology 177 (2011) 353–358 355

Table 3Developmental periods of Hyalomma anatolicum fed on rabbits, sheep and goats (in days).

Developmental stages Rabbits Sheep Goats

Range Mean ± SD Range Mean ± SD Range Mean ± SD

Feeding periods oflarvae

4–5 4.58 ± 0.51 4–5 4.05 ± 0.73 2–5 3.12 ± 0.55

Larval nymphalmolting periods

17–18 17.25 ± 0.45 16–18 17.05 ± 0.71 9–12 10.5 ± 2.12

Hardening periods ofnymphs

7–14 7–14 7–14

Feeding periods ofnymphs

6–8 7 ± 1.15 4–5 4.11 ± 0.32 4–7 4.95 ± 0.58

Nymphal adult moltingperiods

11–14 12.75 ± 1.5 11–14 12.27 ± 1.26 15–17 16 ± 1.4

Hardening periods ofadults

7–14 7–14 7–14

Feeding periods ofadult females

7–11 8.2 ± 1.69 5–7 6.5 ± 0.71 8–11 9.61 ± 1.21

Pre-oviposition periods 4–5 4.8 ± 0.42 5–8 6.1 ± 0.88 4–6 5.17 ± 0.75Pre-eclosion periods 20–24 21.3 ± 1.16 22–24 22.3 ± 0.68 21–24 22.5 ± 1.05Hardening periods of 7–14 7–14 7–14

88–1

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larvaeTotal (average) 90–127 (108.5)

4–5 days, mean 4.11 ± 0.32) and on goats (4–7 days, mean.95 ± 0.58) (Table 3).

Table 3 shows that engorged nymphs detached fromabbits molted within 11–14 days (mean 12.75 ± 1.5)nd those detached from sheep molted within 11–14ays (mean 12.27 ± 1.26). These were significantly shorterP < 0.01) than those detached from goats that moltedithin 15–17 days (mean 16 ± 1.4).

.3. Feeding of adults

Adults female feeding periods ranged from 7 to 11 daysmean 8.2 ± 1.69) on rabbits and from 8 to 11 days (mean.61 ± 1.21) on goats. These were significantly longerP < 0.05) than the 5–7 days (mean 6.5 ± 0.71) feeding peri-ds recorded on sheep (Table 3).

.4. Engorged weights and egg production

As shown in Table 4, in case of rabbits, 10 engorgedemale ticks ranging in weights between 340.6 and39.4 mg (mean 482.92 ± 88.08), produced eggs masseshat ranged in weights between 195.3 and 390.1 mgmean 296.39 ± 59.42) and the estimated numbers of

ggs produced ranged between 3753 and 5987 (mean881.9 ± 842.71). On sheep, 10 engorged female ticksanging in weights between 227.4 and 581.7 mg (mean16.36 ± 107.05) produced eggs masses that weighedetween 114.3 and 372.8 mg (mean 257.66 ± 82.74)

able 4elationships between weights of engorged females Hyalomma anatolicum, their

Host No. ofticks

Weights of engorgedfemales (mg)(mean ± SD)

Weights of eg(mg) (mean ±

Rabbits 10 482.92 ± 88.08 296.39 ± 59.4Sheep 10 416.36 ± 107.05 257.66 ± 82.7Goats 6 211.4 ± 102.5 122.65 ± 91.1

23 (105.5) 84–124 (104)

and the estimated numbers of eggs produced rangedbetween 1898 and 6599 (mean 4274.7 ± 1433.59), whileon goats six engorged female ticks ranging in weightsbetween 51.9 and 294.0 mg (211.4 ± 102.5) producedeggs masses that weighed between 11.01 and 164.9 mg(mean 122.65 ± 91.11) and the estimated numbers ofeggs produced ranged between 172 and 2411 (mean1577.5 ± 921.79).

The ratio between weights of engorged female ticks andthe weights of eggs masses and also the estimated numbersof eggs produced showed a positively linear relationships(r = 0.96, r = 0.95, respectively in case of rabbits; r = 0.96,r = 0.93, respectively in case of sheep and r = 0.99, r = 0.96,respectively in case of goats (Figs. 1 and 2).

3.5. Pre-oviposition periods

The pre-oviposition periods of female ticks detachedfrom rabbits ranged from 4 to 5 days (4.8 ± 0.42) and thosedetached from goats ranged between 4 and 6 days (mean5.17 ± 0.75). These were significantly shorter (P < 0.001)than those of female ticks detached from sheep (range 5–8days, mean 6.1 ± 0.88) (Table 3).

3.6. Pre-eclosion periods

Larvae emerged from eggs of ticks fed on rabbitswithin 20–24 days (mean 21.3 ± 1.6) post the first day ofoviposition. This was significantly shorter (P < 0.01) than

eggs masses, numbers of eggs produced and percentage hatchability.

gs massesSD)

Estimated numbers ofeggs (mean ± SD)

% hatchability(mean ± SD)

2 4881.8 ± 842.71 85 ± 9.944 4274.7 ± 1433.59 91.5 ± 3.871 1577.5 ± 921.79 90.4 ± 11.04

356 B.M. Ahmed et al. / Veterinary Parasitology 177 (2011) 353–358

The relationships between the weights of engorged Hyalomma anatolicum female ticks fed on rabbits,

y = 0.6538x - 19.252r = 0.96 (rabbits).

y = 0.8702x - 162.57r = 0.96 (sheep).

y = 1.1332x - 377.82r = 0.99 (goats).

0

50

100

150

200

250

300

350

400

450

0 100 200 300 400 500 600 700

Tick engorgement weights (mg.).

Egg

s ba

tche

s w

eigh

ts (

mg.

).

Rabbits

Sheep

Goats

Fig. 1. The relationships between the weights of engorged Hyalomma anatolicum female ticks fed on rabbits, sheep, goats and that of eggs they laid.

The relationships between the weights of engorged Hyalomma anatolicum female ticks fed on rabbits and

the numbers of eggs they laid.

y = 9.0882x + 493.05r = 0.95 (Rabbits)

y = 14.032x - 2501.6r = 0.93 (sheep)

y = 15.389x - 4992.8r = 0.96 (Goats)

0

1000

2000

3000

4000

5000

6000

7000

0 100 200 300 400 500 600 700

Tick engorgement weights (mg.).

Est

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Rabbits

Sheep

Goats

Fig. 2. The relationships between the weights of engorged Hyalomma anatolicum female ticks fed on rabbits and the numbers of eggs they laid.

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B.M. Ahmed et al. / Veterinar

hose emerged from eggs of ticks fed on both sheep andoats being 22.3 ± 0.68 and 22.5 ± 1.05 days, respectivelyTable 3).

.7. Hatchability

The hatching percentages among eggs laid by femaleicks fed on goats ranged between 85% and 97% (mean1.5% ± 3.87) and that of eggs laid by ticks fed onheep ranged between 69% and 99% (mean 90.5 ± 11.04).lthough the eggs laid by ticks fed on rabbits recorded

ower percentage hatchability, which ranged between 67%nd 94% (mean 85% ± 9.94), but no significant differenceP > 0.05), were detected compared to ticks fed on sheepnd goats (Table 4).

. Discussion

Although ticks are known to utilize many domestic ani-al species as hosts, there has been little work to show

he influence of hosts on the biology of ticks (Dipeolu andkinboade, 1984). Dipeolu and Adeyefa (1984) showed that

icks (H. rufipes, A. variegatum, R. (B.) decoloratus and R.B.) geigyi), which fed on sheep and horses were not asiologically viable as those of the same tick species thatere fed on cattle. The results of the present investigations

uggested that there are some fundamental differencesetween the biology of H. anatolicum that were fed on rab-its, sheep and goats.

This study showed that the feeding periods of larvaend nymphs on rabbits were significantly (P < 0.001) longerhan those fed on sheep and goats, while the feeding peri-ds of adult female ticks fed on both goats and rabbits wereignificantly (P < 0.05) longer than that of female ticks fedn sheep. On the other hand the pre-oviposition periods ofdult female ticks fed on sheep were significantly longerP < 0.001) than those of female ticks fed on both rabbitsnd goats. However, the pre-eclosion periods of eggs laidy ticks fed on rabbits were significantly shorter (P < 0.01)han those of eggs laid by female ticks fed on either sheepr goats. The low egg production of ticks fed on goatshen compared to that of female ticks fed on both rabbits

nd sheep (Table 4) may indicate that goats show someesistance to adult ticks feeding and may not be favorableost for the tick H. anatolicum. Previous records showedhat goats carry fewer ticks when compared to other hostsDipeolu, 1975; Mwangi et al., 1985; Jongejan et al., 1987).. anatolicum and H. impeltatum represented a very smallercentage (0.9%) of ticks collected from goats during 1990nd formed 7.1% of those collected in 1991 (Al-Khalifa et al.,007).

The present study showed also that 94.13% of H.natolicum larvae underwent a 2-host cycle on rabbits.pparently this is not in agreement with the findings ofassir et al. (1992) who found this tick to behave as a typi-al 3-host tick on rabbits, but it is in line with that reported

y Hosie and Walker (1979), who reported that 98% of the

arvae of this tick species behaved as a 2-host tick. How-ver, other workers reported variable percentages (46.6%nd 25%) of this partial 2-host cycle in this tick species whened on rabbits (Latif, 1985; El Ghali et al., 2003).

tology 177 (2011) 353–358 357

Only 6.33% and 24.33% of H. anatolicum larvae were ableto complete feeding as 3-host life cycle on sheep and goats,respectively. However, larvae that were likely to under go2-host life cycle failed to complete molting on these hosts.This phenomenon was reported by many workers. Neitz(1972) stated that “although larvae of both Rhipicephalusbursa and Rhipicephalus evertsi mimeticus readily attachedon the ears of sheep, the nymphal harvests were very poor.The reason for this was attributed to the inclination of lar-vae to attach in large numbers at localized areas at the baseand other sites of the inner surface of the ear. As feedingprogressed a variable degree of suppuration developed atattachment sites. Many of the engorged larvae and othersin the process of molting were then smothered by the exu-dates from the cutaneous lesions”. A similar phenomenonwas noticed by Hoogstraal (1956) and Yassir et al. (1992)with Amblyomma lepidum larvae when fed on rabbits. Thelater author attributed this pre-molting death to humidityfactor rather than lethal factors in rabbit’s blood.

The feeding periods of larvae of the tick H. anatolicumfed rabbits, sheep and goats (Tables 1 and 3) did not dif-fer radically from those reported by El Ghali et al. (2003)and Yassir et al. (1992) working on the same species fed onrabbits. They found the larvae of this tick species to feed for2–3 days and for 4–5 days, respectively.

In the present study, the feeding periods of nymphs onrabbits ranged between 6 and 8 days which was signifi-cantly longer (P < 0.001) than that of nymphs fed on bothsheep and goats (4–5 and 4–7 days, respectively). The feed-ing periods of nymphs on sheep and goats agreed with thatreported by El Ghali et al. (2003), but it was shorter thanthat (4–8 days) reported Yassir et al. (1992), when this tickspecies fed on rabbits and it is shorter than that (4–8 days)reported by Osman (1999) when nymphs fed on sheep.

The adult females of the tick H. anatolicum fed for 8–11days on goats and for 7–11 days on rabbits. These peri-ods were significantly longer (P < 0.05) than that of adultfemale fed on sheep which recorded 5–7 days. Yassir et al.(1992) and El Ghali et al. (2003) reported a feeding periodof the adult females of the tick H. anatolicum on rabbits tobe 5–8 days which is in line with the feeding periods ofadult females fed on sheep in this study, but it is shorterthan that reported by Osman (1999) who found the adultfemales of this tick to feed for 5–10 days on sheep.

There is a general acceptance of the concept that theweights and numbers of eggs laid by a tick are directlyrelated to the weight of the engorged female tick (Snowand Arthur, 1966). This relationship was proved by manyworkers in many tick species (e.g. Londt, 1977; Norval et al.,1980; Dipeolu and Ogunji, 1980; Dipeolu, 1983; El Ghaliet al., 2003). This was confirmed in the present study, inwhich this relationship was found to be linearly positivebetween the weights of the engorged females and theireggs masses (Fig. 1).

Engorgement weights of some female ticks in Africawere studied by Dipeolu (1989). He found that engorge-

ment weight in different Hyalomma species may reach up to0.97 g, which was much higher compared with the resultsof the present study, in which the highest engorgementweight of a female tick was found to be 0.639 g on rab-bits. The low engorgement weights of female ticks fed on

ry Parasi

Winston, P.H., Bates, D.H., 1960. Saturated solutions for the control of

358 B.M. Ahmed et al. / Veterina

goats may indicate that they are not the preferable hosts ofadults of H. anatolicum (Table 4). This is further confirmedas mentioned earlier by the fact that in the present studythe ovipositional capacities of female ticks fed on rabbitsand sheep were much higher when compared with thatof female ticks fed on goats. The average numbers of eggsproduced by ticks fed on rabbits and sheep was found tobe 4881.8 and 4274.7, respectively (Table 4). Yassir et al.(1992) found similar ovipositional capacities of this tickspecies when fed on rabbits.

A serological survey by Taha et al. (2003) revealedthat 20% of goats in River Nile State/Sudan were positivefor T. lestoquardi antibodies. However, no clinical cases ofmalignant ovine theileriosis (MOT) were reported in thisanimal species even when their sheep mates were severelyaffected with MOT. T. lestoquardi was successfully transmit-ted from sheep to goats and vice versa using H. anatolicum(Taha, 2000). Hence the successful feeding of even a smallportion of H. anatolicum on goats may complicate the epi-demiology of MOT in areas where sheep and goats areraised together.

Finally, the present study indicated the ability of H. ana-tolicum to complete its life cycle on various host speciesunder laboratory conditions. The present study also indi-cates that goats may not be the preferable host for H.anatolicum. To our knowledge this also represents the firstreport of studying the life cycle of H. anatolicum or for thatmatter of any tick species on goats in Sudan.

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