Life cycle of the camel tick Hyalomma dromedarii (Acari: Ixodidae) under field conditions in Northern Sudan

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  • Veterinary Parasitology 174 (2010) 305312

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    Veterinary Parasitology

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

    Life cyc medunder

    A. ELGhaa Central Veterb Department o n

    a r t i c l e i n f o

    Article history:Received 12 April 2010Received in reAccepted 23 A

    Keywords:Camel tickHyalomma droLife cycleSudan

    a b s t r a c t

    Engorged Hyalomma dromedarii females were placed for development in shade and sun

    1. Introdu

    The entiis mainly aity (BranagaPegram andand moultitive humidi

    CorresponE-mail add

    0304-4017/$ doi:10.1016/j.vised form 10 August 2010ugust 2010


    (open non-shaded site) in April, August and December for two successive years. Engorgednymphs were also placed at the same sites in January, March, May, June, July and August.Preoviposition periods ranged between 9.8 and 11.7 days in the shade but longer in the sunin December (14.7 days). Egg production index was higher in August (0.72) than in Apriland December (0.46 and 0.39, respectively) in shade and in August compared to Decemberin the sun (0.65 and 0.29, respectively). In shade and in sun, the prehatching periods werelonger in December (50.7 and 48.2 days) than in April and August (25.6 and 29.0 days).Percentage hatchability ranged between 82 to 94.1% and 56.2 and 58.9% in the shade andsun, respectively. Number of eggs laid and eggs hatched were positively correlated withfemales engorgement weights. There were high mortality rates of females in the sun andmost of the eggs desiccated. Slight increased ambient and soil temperatures increased eggproduction, shortened preoviposition periods and decreased hatchability while increasedhumidity shortened preoviposition and prehatching periods and increased hatchability.

    Nymphaladult moulting periods were long in January (20.7 days in the shade and 14.4days in the sun) and short in August in the shade (7.8 days) while they were only 6 days inMayand June in the sun.Highnumbersmoulted inallmonths in the shade (ranges23.329.5nymphs). The mean mortality of engorged nymphs in the shade was very low. However,in the sun mortality was high (12.930 nymphs). Premoulting periods were negativelycorrelatedwith ambient temperature but positively correlatedwith humidity. In the shade,mean number of nymphs moulting increased with increased mean ambient temperature,humidity and rainfall.

    Published by Elsevier B.V.


    re life cycle or developmental period of ticksffected by temperature and/or relative humid-n, 1973a,b; Tukahirwa, 1976; King et al., 1988;Banda, 1990). Egg production index, hatching

    ng percentages are also temperature and rela-ty dependant (Norval, 1977; Zahler and Gothe,

    ding author. Tel.: +00 249 09 12805583.ress: (A. ELGhali).

    1995; ELGhali et al., 2003). Life cycle of the camel tickHyalomma dromedarii has only been studied under labo-ratory conditions (Hagras and Khalil, 1988; Alahmed andKheir, 2003). This tick species follows different types oflife cycles to avoid unfavourable conditions. Delpy andGouchey (1937 cited in Hoogstraal, 1956) stated that H.dromedarii is a three-host tick, changes to two-host understress of heat to avoid larval desiccation. Alfeev (1951, citedin Hoogstraal, 1956), reported that H. dromedarii behavedas a singlehost on rabbitswith adultsmoving to anewposi-tion shortly after moulting and remaining unattached fora day or two. Hoogstraal (1956) reported that eld obser-

    see front matter. Published by Elsevier B.V.vetpar.2010.08.028le of the camel tick Hyalomma droeld conditions in Northern Sudan

    lia,, S.M. Hassanb

    inary Research Laboratories, P.O. Box 8067, Amarat, Khartoum, Sudanf Parasitology, Faculty of Veterinary Medicine, University of Khartoum, Sudaarii (Acari: Ixodidae)

  • 306 A. ELGhali, S.M. Hassan / Veterinary Parasitology 174 (2010) 305312

    vations suggested that change of host usually occurs afternymphaladult moulting and rarely after larvalnymphalmoulting. Das and Subramanian (1972) reported that H.dromedarii on sheep and cattle is a three-host tick and 60%changed topointed outhostwhen tand Kheir (host tickwh(2010) founwhen fed ois distributpresent, inEast, inNordown to So1956). It re(Karrar et aet al., 2001importanceare importhealth andThe presendromedariibest periodThe effectssun on the

    2. Materia

    The stuAtbara towNile State,and River A(Fig. 1). The45 C in sumambient temto less thanis generallybetween 30and 30 C in

    Two areMinimum ahumidity arecorded atalso recordewere measu

    2.1. Eggs la

    Fully enfrom cameplaced in 7wool and diately placwith an appof 1520 relar numberout in Dece2002, Aprilsion periodand hatched

    of total eggs produced by each female small batches of eggswere weighed and counted and accordingly the total eggswere estimated. By the end of hatching, larvae or the non-hatched eggs were counted and calculated as percentage

    the to


    at larvdingrged nclosedlacedk laye. The v. This, May,


    preovns andbefor

    ata wel (GLMAS parianceed usin(REGWrequirbeforhatchaon anlopmelopme


    ean dasion aare

    highesDecemand oable 2halats winigheseenwar excethe mumberbatche, werDecemwas neen Au.001) hemalesds rangnicatwo-host when fed on rabbits. Ouheli (1994)that this tick is a three-host changing to two-heirdensityon thehostbecomeshigh.Alahmed2003) reported that this tick behaved as a two-en fed on rabbits. Recently, ELGhali andHassand that this tick behaved as a two-host tickn camels in Northern Sudan. This tick speciesed throughout the world wherever camels aresouthern Russia, in the Far, Middle and NearthAfrica and south of the great northern desertsmalilands and northeastern Kenya (Hoogstraal,presents nearly 90% of ticks infesting camelsl., 1963; Van straren and Jonjegan, 1993; Diab; ELGhali and Hassan, 2009). The economicof this tick species is considered as the camels

    ant exporting animals in the Sudan and theirproduction are affected by high tick infestation.t work was conducted to study development H.under natural conditions aiming to identify thes of the tick development in Northern Sudan.of temperature, relative humidity, shade anddevelopmental periods are studied.

    ls and methods

    dy was conducted under eld conditions inn (Long. 3358E and Lat. 1740N) in RiverNorthern Sudan (at the junction of River Niletbara) where camels are reared and marketedmeanmaximumambient temperature is aboutmer (March to June) and the mean minimumperature in winter (October to February) falls10 C. The mean ambient relative humiditylow while the mean soil temperature rangesand 55 C in summer and ranges between 15winter.

    as were divided into two sites shaded and open.nd maximum ambient temperatures, relativend soil temperature at ground level were daily09:00 and 15:00h and total daily rainfall wasd. In this aspect all thesemeteorological factorsred closely to the tested ticks.

    ying and hatching

    gorged H. dromedarii females were collectedls and immediately weighed and individually.5 cm2.5 cm glass vials, closed using cottonxed with adhesive tape. The vials were imme-ed in the eld at a depth of 35 cm and coveredroximately uniform thick layer of litter. A totalplicates were placed in the shade and a simi-in the sun at each area. This study was carriedmber 2001, April 2002, August 2002, December2003 and August 2003. Preoviposition, preeclo-s were daily recoded and number of eggs laidfor each female was estimated. For estimation



    Flaccorengovials,andpa thicarea)tality2003



    Dmodethe Sof vaformtesteverscale(e.g.relatidevedeve

    3. Re

    Movipoyearsandfromlowber. Tnympresenand hbetwsimility in


  • A. ELGhali, S.M. Hassan / Veterinary Parasitology 174 (2010) 305312 307

    periods wecompared tin the sun, wcompared twashigherengorgemelated with(Table 4).Fig. 1. Sudan map showing Atbara (study area) location and a part of

    re signicantly (P

  • 308A.ELG




    174 (2010) 305312

    Table 1Averages of daily recorded meteorological factors during H. dromedarii oviposition and hatching experiments.

    Periods Min. temperature (C) Max. temperature (C) Soil temp. (C) (9:00h) Soil temp. (C) (15:00h) Rh. (%) (9:00h) Rh. (%) (15:00h) Rain (mm)

    Year 1 Year 2 Year 1 Year 2 Year 1 Year 2 Year 1 Year 2 Year 1 Year 2 Year 1 Year 2 Year 1 Year 2

    DecemberMarch 18.1 16.1 38 37.4 27.7 26.1 43.8 43.8 56.3 35.7 49.3 30.8 0 0AprilJune 26 30.3 46.7 45.2 33.6 32.2 50.8 49.5 38.3 25.5 31.4 22 0 0AugustSeptember 28.5 29 45.7 42.3 35.4 32.7 49.3 42.7 49.1 53.6 31.2 38.4 0.04 1.4

    Rh, relative humidity.

    Table 2Averages of daily recorded meteorological factors during nymphaladult moulting experiments.

    Month Min. temperature (C) Max. temperature (C) Soil temp. (C) (9:00h) Soil temp. (C) (15:00h) Rh. (%) (9:00h) Rh. (%) (15:00h) Rain (mm)

    January 2002 12.3 30.5 20.2 36.7 58.7 40.9 0March 2003 16.1 37.3 26.1 43.8 35.7 30.8 0May 2004 25 48.2 35.9 51.6 24.2 14.2 0June 2004 27.4 46.3 35.2 51.3 32.9 18.3 0July 2004 27.2 45.6 35.6 51.3 36.6 21.9 0August 2004 28.5 45.5 35.8 51.1 43.6 23.1 0.9

    Rh, relative humidity.

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