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

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Veterinary Parasitology 174 (2010) 305312Contents lists available at ScienceDirectVeterinary Parasitologyjourna l homepage: www.e lsev ier .com/ locate /vetparLife cyc medunder A. ELGhaa Central Veterb Department o na r t i c l e i n f oArticle history:Received 12 April 2010Received in reAccepted 23 AKeywords:Camel tickHyalomma droLife cycleSudana b s t r a c tEngorged Hyalomma dromedarii females were placed for development in shade and sun1. IntroduThe entiis mainly aity (BranagaPegram andand moultitive humidi CorresponE-mail add0304-4017/$ doi:10.1016/j.vised form 10 August 2010ugust 2010medarii(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.ctionre 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, hatchingng 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 Sudanlia,, S.M. Hassanbinary 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) 305312vations 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 the2. MateriaThe stuAtbara towNile State,and River A(Fig. 1). The45 C in sumambient temto less thanis generallybetween 30and 30 C inTwo areMinimum ahumidity arecorded atalso recordewere measu2.1. Eggs laFully enfrom cameplaced in 7wool and diately placwith an appof 1520 relar numberout in Dece2002, Aprilsion periodand hatchedof 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 percentagethe toMoultiat larvdingrged nclosedlacedk laye. The v. This, May,Statistipreovns andbeforata wel (GLMAS parianceed usin(REGWrequirbeforhatchaon anlopmelopmesultsean dasion aarehighesDecemand 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 camelsant 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 and methodsdy 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 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 hatchinggorged 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 estimationfrom2.2.Flaccorengovials,andpa thicarea)tality20032.3.InseasobinedDmodethe Sof vaformtesteverscale(e.g.relatidevedeve3. ReMovipoyearsandfromlowber. Tnympresenand hbetwsimility inN(eggshadandtherebetw(PA. ELGhali, S.M. Hassan / Veterinary Parasitology 174 (2010) 305312 307periods wecompared tin the sun, wcompared twashigherengorgemelated with(Table 4).Fig. 1. Sudan map showing Atbara (study area) location and a part ofre signicantly (P308A.ELGhali,S.M.Hassan/VeterinaryParasitology174 (2010) 305312Table 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 2DecemberMarch 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 1.4Rh, 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 0.9Rh, relative humidity.A. ELGhali, S.M. Hassan / Veterinary Parasitology 174 (2010) 305312 309Table3Means(SE)ofdevelopmentalperiodsofH.dromedariiengorgedfemalesundereldconditionsinAtbara,NorthernSudan.SiteMonthNumberofeggsEng.fem.mortality(%)Preovipositionperiod(days)EggproductionindexPrehatchingperiod(days)NumberofeggshatchedHatchability(%)ShadeApril4972.4300.0b(79)1.311.70.6a(79)0.460.03b(79)29.90.4b(51)4226.2365.1a(51)85.12.7a(51)August6932.6383.3a(76),guresinparenthesis=numberofticks.the shade signicantly increasedwith the increase inmeanminimum temperature and rainfall (Table 5) and therewasa signicant positive correlationwith increase inmean soiltemperature at 09:00h. Although preoviposition periodsin the shadedata with thtemperaturdata were nin the sunmeteorologity at 15:00Premoulnicantly lofrom May tlonger in JMarch, Julyin May andwasnot signtion of Marvery low buThe premwere signiimum, minsignicantl09:00 and 1humidity inof nymphs aambient anmoulting ra4. DiscussiEffect ocantly diffeovipositeddied in fewthe hot monin this studviduals couThis mightthese indivditions. Eggwere foundin the shaddry monthssustained ding, also, hand Hassan(89.9% H. dthe yearwitber. Patrickpreovipositperature welevates. Hasition of H.decreased fsition perioAugust, butwhich seemence may brainfall of awere negatively correlated with meteorologice exception of maximum temperature and soile at 15:00h but in the sun othermeteorologicalegatively correlated. Mean number of eggs laidwas signicantly positively correlated with allical data with the exception of relative humid-h.ting periods of nymphs in the shade were sig-nger in January followed byMarch and shortero August (Table 6). Premoulting in the sun wasanuary but was not signicantly different inand August. The shortest period was recordedJune. Number of nymphs moulted in the shadeicantlydifferent in allmonthswith theexcep-ch. Mean mortality of nymphs in the shade wast was very high in the sun.oulting periods in the shade and in the suncantly negatively correlated with mean max-imum and soil temperatures (Table 7) buty positively correlatedwith relative humidity at500h.With increased temperature and relativethe shade, there was an increase in moultingnd decrease inmortality rate. Increase inmeand soil temperatures in the sun led to a decreasedte and an increased mortality rate.onf shade and sun on oviposition was signi-rent. While all engorged females under shadeand most eggs hatched, most of the femalesdays before laying of eggs in the sun duringths. It was noticed that although all ticks usedy were from the same population, few indi-ld escape the adverse conditions in the controlled by some intrinsic factors allowediduals to resist the unfavourable climatic con-s laid in the sun in December and August 2003desiccated due to low relative humidity bute hatchability rate was high even during hot. This implies that tick population in nature isespite adverse climatic conditions. This nd-elps to explain the observations of ELGhali(2009), at the same study area, in that ticksromedarii) were found on camels throughouth the highest infestation duringMarch to Octo-and Hair (1979) and Punyua (1984) found thation periods of tickswithin the permissible tem-ere found to shorten as ambient temperaturegras and Khalil (1988) reported that preovipo-dromedarii was prolonged as the temperaturerom 34 to 21 C. In the current study, preovipo-d was longer in December and April than inthe difference was not signicant in the shades to minimize the effect of heat. This differ-e attributed to the fact that in August 2003,bout 22mm was recorded leading to a rise in310 A. ELGhali, S.M. Hassan / Veterinary Parasitology 174 (2010) 305312Table 4Correlation analysis among H. dromedarii engorged female developmental periods in the shade and in the sun in Atbara, Northern Sudan.Site Parameters Number of eggs Preoviposition periods Prehatch. Period Hatchability (%)Shade (174) Engorged weight 0.43*** 0.07NS 0.04NS 0.36***Number of eggs 0.18* 0.45*** 0.88***Preoviposition Period 0.63*** 0.26***Prehatching period 0.45***Sun (17) Engorgement weight 0.32NS 0.43NS 0.1NS 0.13NSNumber of eggs 0.2NS 0.4NS 0.02NSPreoviposition Period 0.15NS 0.22NSPrehatching period 0.11NSNS=not signicant, gures in parenthesis =number of ticks.* PA. ELGhali, S.M. Hassan / Veterinary Parasitology 174 (2010) 305312 311Table 7Correlation analysis between H. dromedarii nymphaladult moulting periods and meteorological values in the shade and in the sun in Atbara, NorthernSudan.Site Met. data Premoulting period Number moulted Number diedShade (190) *** * *Sun (43)Data without sMin=minimu 15:00h, Rh3 rged ny* P0.05.*** P0.001Periodshumidity de1990; Hass2003). PrehsignicantlEgg hatchawas higherApril in theshade wasand subseqbility (RechMohammedthat life cycand hatchinmentweighcorrelationand prehattion of suitthis tick spcorrelationto the unfavsample sizealtered thePremoulaffected byreported thopen condimoulting pbut this facdue to theture of themoulting pin March anhigher in Jain other motemperaturdevelopingmoulting wthe shade ae interureswds. Coeraturlated waximissibles.wasdity hdevelobe duee soil tin thet valuee resuns leaabilityes tolossesrged stMin. 0.92Max. 0.95***Soil9 0.96***Soil3 0.96***Rh9 0.76***Rh3 0.92***Rain 0.2***Min. 0.69***Max. 0.80***Soil9 0.78***Soil3 0.80***Rh9 0.77***Rh3 0.81***Rain 0.26tars are not signicant.m temperature, Max=maximum temperature, Rh9= relative humidity at= relative humidity at 15:00h. Numbers in parenthesis =number of engoof egg hatching are temperature and relativependent (Short et al., 1989; Pegram and Banda,an, 1997; Mohammed, 2002; ELGhali et al.,atching periods of eggs in the current studywasy longer in December than in April and August.bility was mainly affected by the site where itin the shade than in the sun. All females died insunwhile hatchability in the samemonth in thethe highest. Heat leads to water loss from eggsuently leads to desiccation and decreased via-av and von Maltzahn, 1977; Diehl et al., 1982;, 2002). Alahmed and Kheir (2003) reportedle of H. dromedarii depends on egg productiong. The positive correlation between engorge-ts of females and eggnumbers and the negativeof these two parameters with preovipositionching periods obtained in this study is a func-able conditions that favoured the fecundity ofecies under eld conditions. The insignicantbetween these parameters in sun may be dueourable situation in the sun although the smallabovperatperiotempcorrethat mpermmentIthumiwithmayas thversaferenThseasohatchspecihighengo(17), due to death ofmost samples, might haveresults.ting periods and moulting percentage areseasons. Dipeolu (1984) and Hassan (1997)at the premoulting periodwas shortened undertions than in the shade. In the sun, the pre-eriod was slightly shorter than in the shade,t was reversed in July and August. This may befact that there was no difference in tempera-shade and sun during the rainy months. Theercentage was signicantly lower in the shaded higher in other months but in the sun it wasnuary andMarch while almost all nymphs diednths. This nding conrms the fact that highe and low humidity lead to loss of water fromstages leading to desiccation. The nding thatas positively correlated with temperature innd with humidity in both sites supports thein control sthe drop-ofto be betweallowed toReferencesAlahmed, A.M(Acari: Ixo1114.Bailey, K.P., 19and their iBull. Epiz.Bennett, F.G.,(Acarida: IAcarologiaBranagan, D.,of the ixounder Qua5, 153160.18 0.140.1 0.020.11 0.10.1 0.0040.1 0.18*0.001 0.10.1 0.10.34* 0.30.35* 0.30.36* 0.3*0.37* 0.32*0.31* 0.270.35* 0.31*0.22 0.24Soil9 = soil temperature at 09:00h, Soil3 = soil temperaturemphs batches.pretation. In the sun in this study both tem-ere negatively correlatedwith the premoultingncerning the number moulted, the minimume unlike maximum temperature was positivelyith them. This could be explained by the factum temperature in the sun usually exceeds thetemperature that favours moulting require-observed that soil temperature and relativead approximately the same correlation resultspment parameters at 9:00 and 15:00h. Thisto the fact that the relative humidity increasesemperature decreases in the morning and viceafternoon. This relationship is xed with dif-s in different seasons.lts of high fecundity in the shade during allding to high egg production, high per centand high per cent moulting enable this tickavoid adverse effects of the climate in whichoccur among the host-seeking stages. Death ofages of this tick species in sunmay be of benettrategies. ELGhali and Hassan (2010) reportedf rhythms ofH. dromedarii females and nymphsen 18:00 and 20:00h and hence camels can bespend all or part of the nights at open areas.., Kheir, S.M., 2003. Life cycle and survival of H. dromedariididae) under laboratory conditions. Agric. Mar. Sci. 8 (1),60. Notes on the rearing of Rhipicephalus appendiculatusnfectionwith Theileria parva for experimental transmission.Dis. Afr. 8, 3343.1974. Oviposition of Boophilus microplus (Canestrini)xodidae). II. Inuence of temperature, humidity and light.1.6 (2), 250257.1973a. Observations on the development and survivaldid tick Rhiphicephalus appendiculatus Neumann, 1901si-Natural conditions in Kenya. Trop. Anim. Health Prod.5.312 A. ELGhali, S.M. Hassan / Veterinary Parasitology 174 (2010) 305312Branagan, D., 1973b. The developmental periods of the ixodid tick Rhipi-cephalus appendiculatus Neum. under laboratory conditions. Bull.Entomol. Res. 63, 155168.Das, H.I., Subramanian, G., 1972. Biology of Hyalomma dromedarii Koch,1844 (Acari: Ixodidae). Indian J. Anim. Sci. 42, 285289.Day, R.W., Quinn, G.P., 1989. Comparison of treatments after analysis ofvariance in ecology. Ecol. Monogr. 59 (4), 433463.Diab, F.M., ELkady,G.A., Shouky,A., 2001. Bionomics of ticks collected fromSinai. 2. Abundance, attachment sites and density of ticks infestingArabian camels. J. Egypt. Soc. Parasitol. 31, 479489.Diehl, P.A, Aeschlimann, A., Obenchain, F.D., 1982. Tick reproduction,oogenesis and oviposition. In: Obenchain, F.D., Galun, R. (Eds.), Phys-iology of Ticks. Pergamon Press, New York, pp. 277350.Dipeolu, O.O., 1984. Development of ixodid ticks under natural conditionsin Nigeria. Trop. Anim. Health Prod. 16, 1320.ELGhali, A., Hassan, S.M., 2009. Ticks (Acari: Ixodidae) infesting camels(Camelus dromedarius) in Northern Sudan. Onderstepoort J. Vet. Res.76, 177185.ELGhali, A., Hassan, S.M., 2010. Drop-off rhythms and survival periodsof Hyalomma dromedarii (Acari: Ixodidae) fed on camels (Camelusdromedarius) in the Sudan. Vet. Parasitol. 170, 302306.ELGhali, A., Osman, O.M., ELRabaa, F.M.A., 2003. Some studies on biolog-ical behaviour of H. a. anatolicum (Acari: Ixodidae) under laboratoryconditions. I. Development. Sud. J. Vet. Sci. Anim. Husb. 42 (1 and 2),7288.Hagras, A.E., Khalil, G.A.M., 1988. Effect of temperature on Hyalommadromedarii Koch (Acari: Ixodidae). J. Med. Entomol. 25 (5), 354359.Hassan, S. M., 1997. Ecological studies on R. appendiculatus and A. var-iegatum (Acari: Ixodidae): drop-off rhythms, development, survivaland seasonal population dynamics. Ph.D thesis, Kenyatta University,Kenya. 206 pp.Hoogstraal, H. (1956). African Ixodoidea. 1. Ticks of the Sudanwith specialreference to Equatoria Province and with preliminary reviews of thegenera Boophilus, Margaropus and Hyalomma. U.S. Navy WashingtonD.C. 1101 pp.Karrar, G., Kaiser, M.N., Hoogstraal, H., 1963. Ecol ogy and host-relationship of ticks (Ixodoidea) infesting domestic animals in KassalaProvince, Sudanwith special reference toAmblyomma lepidumDonitz.Bull. Entomol. Res. 54, 509522.King,D.,Getting,Newson,R.M., 1988.Aclimate-basedmodel for thedevel-opment of the ixodid tick, Rhipicephalus appendiculatus in East Coastfever zones. Vet. Parasite 29, 441451.Mohammed, A.S., 2002. Bioecological studies on the tick A. lepidum(Donitz, 1909) under natural eld conditions in BlueNile State, Sudan.Ph.D thesis, U. of K, Sudan.Norval, R.A.I., 1977. Studies on the ecology of the tick Amblyommahebraeum Koch in Eastern Cape Province of South Africa. II. Survivaland development. J. Parasitol. 63, 740747.Ouheli, H., 1994. Comparative development of Hyalomma marginatum(Koch, 1844),H. detritum (Schulze, 19919),H. lusitanicum (Koch, 1844)andH. dromedarii (Koch, 1844) under laboratory conditions. Acta Par-asitol. 39 (3), 153157.Patrick, C.D., Hair, J.A., 1979. Ovipostion behaviour and larval longevityof the lone star tick, (A. americanum) (Acarina: Ixodidae) in differenthabitats. Entomol. Soc. Am. 72 (2), 308312.Pegram, R.G., Banda, D.S., 1990. Ecology and phenology of cattle ticks inZambia: development and survival of free living stages. Exp. Appl.Acarol. 8, 291301.Punyua, D.K., 1984. Development periods of Rhipicephalus appendiculatusNeumann (Acarina: Ixodidae) under eld conditions. Insect Sci. Appl.5 (4), 247250.Rechav, Y., von Maltzahn, H., 1977. Hatching and weight changes in eggsof two species of ticks in relation to saturation decit. Ann. Entomol.Soc. Am. 70 (5), 768770.Short, N.J., Floyd, R.B., Norval, R.A.I., Sutherst, R.W., 1989. Developmentrate, fecundity and survival of developmental stages of the ticks R.appendiculatus, B. decoloratus and B. microplus under eld conditionsin Zimbabwe. Exp. Appl. Acarol. 6, 123141.Sweatman, G.K., 1967. Longevity and oviposition of engorged Rhipi-cephalus sanguineus female ticks. J. Parasitol. 53 (2), 432445.Tukahirwa, E.M., 1976. The effect of temperature and relative humidity onthe development of R. appendiculatus Neumann (Acarina: Ixodidae).Bull. Entomol. Res. 66, 303312.Van straren, M., Jonjegan, F., 1993. Ticks (Acari: Ixodidae) infesting theArabian camel (Camelus dromedarius) in Sinai, Egypt with a note onacaricidal efcacy of ivermectin. Exp. Appl. Acarol. 17, 605612.Zahler, M., Gothe, R., 1995. Effect of temperature and humidity on egghatching, moulting and longevity of larvae and nymphs of Dermacen-tor reticulatus (Ixodidae). Appl. Parasitol. 36, 5365.Life cycle of the camel tick Hyalomma dromedarii (Acari: Ixodidae) under field conditions in Northern SudanIntroductionMaterials and methodsEggs laying and hatchingMoulting periods of nymphs to adultsStatistical analysisResultsDiscussionReferences


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