Population dynamics of infesting in the arid steppes of

Khawla Elati1* Ayet Allah Ayadi1 Médiha Khamassi Khbou2 Mohamed Jdidi1 Mourad Rekik3 Mohamed Gharbi1

Keywords Summary Sheep, Metastigmata, This study aimed to determine population dynamics infesting sheep in Gafsa sanguineus sensu lato, Hyalomma region (Central Tunisia). Ticks were collected monthly over a year, from Octo- excavatum, population dynamics, ber 2013 to September 2014, from 57–64 randomly-included Barbarine-breed Tunisia sheep. In total, 560 ticks were collected and identified. They belonged to two species: Rhipicephalus sanguineus sensu lato (98.6%) and Hyalomma excava-

Submitted: 1 April 2017 tum (1.4%). Sheep were only infested from April to October with a maximum ANIMALE ET ÉPIDÉMIOLOGIE ■ SANTÉ Accepted: 29 August 2018 infestation prevalence (number of infested / number of examined ani- Published: 29 October 2018 mals) in August for R. sanguineus s.l. (83%), and in May for H. excavatum (7%). DOI: 10.19182/remvt.31641 The highest infestation intensity (number of ticks / number of infested sheep) was 3.7 ticks per in August. These results should help sheep owners and vet- erinarians to implement efficient control programs against ticks and the patho- gens they transmit.

■ How to quote this article: Elati K., Ayadi A.A., Khamassi Khbou M., Jdidi M., Rekik M., Gharbi M., 2018. Population dynamics of ticks infesting sheep in the arid steppes of Tunisia. Rev. Elev. Med. Vet. Pays Trop., 71 (3): 131-135, doi: 10.19182/remvt.31641

■ INTRODUCTION (Rjeibi et al., 2016b), Babesia ovis (Rjeibi et al., 2014) and Anaplasma ovis (Ben Said et al., 2015). Agriculture and most particularly extensive livestock production Climate change is an important emerging risk factor affecting agri- are vital for the livelihood of small landholders on the Southern culture, human and livestock health (Keleman Saxena et al., 2016). Mediterranean shore. Sheep breeding is a major breeding activity This is particularly true in North Africa considered as a “hot spot in Tunisia. Its development is threatened by numerous constraints for climate change” (Giorgi, 2006). Increases in temperature cause such as diseases, in particular tick-borne diseases. Ticks can cause heat stress in livestock species, hence provoking reductions in hypersensitivity, inflammation and anemia impairing animal pro- growth rate, milk yield and reproductive performance (Das et al., ductivity. They also transmit several pathogens (parasites, bacteria 2016). Furthermore, these changes affect the spread and abundance and viruses), that can result in a high cost from loss of infected ani- of several vector such as ticks, mosquitoes and flies, mals (Gharbi and Darghouth, 2014). In Tunisia, several of these ticks leading to a modified transmission of several pathogens (Elbers et transmit pathogens to sheep with various prevalence and veterinary al., 2015). The proliferation of vector ticks caused by the tempera- importance: Theileria ovis (Rjeibi et al., 2014), Theileria lestoquardi ture increase promotes the emergence of various diseases such as Crimean-Congo hemorrhagic fever (Leblebicioglu et al., 2015). More precisely, increases in temperature might on one hand provide a suit- able environment for the spread of thermophilic tick species such as 1. Laboratoire de parasitologie, Univ. Manouba, Institution de la recherche et de Hyalomma marginatum and Rhipicephalus annulatus (Domșa et al., l’enseignement supérieur agricoles, Ecole nationale de médecine vétérinaire de Sidi Thabet, 2020 Sidi Thabet, Tunisie. 2016), and, on the other hand, result in the population decrease of 2. Laboratoire de maladies contagieuses-zoonoses, législation sanitaire, Univ. species which prefer more temperate conditions, e.g. Ixodes ricinus. Manouba, Institution de la recherche et de l’enseignement supérieur agricoles, Ecole nationale de médecine vétérinaire de Sidi Thabet, 2020 Sidi Thabet, Tunisie. Under such epidemiological and changing climate conditions, the 3. International Center for Agricultural Research in the Dry Areas (ICARDA), study of tick infestation dynamics in sheep is crucial. The implemen- Amman 11195, . tation of any tick control and, subsequently, tick-borne pathogen con- * Corresponding author trol programs cannot succeed if no specific data are available regard- Tel.: +216 71 552 200; Fax: +216 71 552 441; Email: [email protected] ing the seasonal prevalence and local phenology of the tick species concerned. This study reports, for the first time to our knowledge,

https://creativecommons.org/licenses/by/4.0/ tick infestation dynamics in sheep in arid Tunisian steppes. tropicaux, 2018, 71 (3) : 131-135 des pays et de médecine vétérinaire Revue d’élevage 131 132 Revue d’élevage et de médecine vétérinaire des pays tropicaux, 2018, 71 (3) : 131-135 ■ SANTÉ ANIMALE ET ÉPIDÉMIOLOGIE Seasonal activityofticksinfestingsheepinTunisia Tick infestation intensity = intensity Tick infestation sheep) examined (%) prevalence = Infestation al., et 1982): (Margolis indicators parasitological two using expressed were 2016). al., Results et moğlu the with Student t test. Results were considered significant at5% threshold. significant considered were Results ttest. Student with out al.,et 2011). carried were means of infestation tick Comparison (Dean software Epi-Info with performed were tests chi-square months, and gender age groups, between prevalence To infestation compare sanguineus lus Rhipicepha between (2003). similarities of morphological Because Walker to al. et according identified then were 10% They glycerine. and 70% ethanol containing flasks labeled in collected were ticks and examined 2014. thoroughly were sheep tember surveyed All 2013 October for year, one from Sep monitored to were sheep The May). (in at2.5‰ ayear once non formulation adiazi with ectoparasites against treated were Animals period. ing low the graz during barns in kept were Males suckling. early during and of end pregnancy atthe before mating, supplemented were Ewes system. breeding a semi-intensive under kept were and tures pas natural on day the during (over old). grazed ayear sheep The old) year one oradult than (less young as classified were animals survey. Selected the in included were animals, 400 comprising flock Each month, a sample of 57‒64 sheep, (0°C). February and January in randomlyrecorded chosen is within temperature minimum mean a The of summer. 49°C in maximum a reach can temperatures and September to April from extends period dry the region, this In of millimeters. 200 rainfall annual Tunisia amaximum with of Central steppes of arid the typical is ity (34° 25’ District locality, Sned Gafsa out in carried was survey current The ■ MATERIALSMETHODS AND ticks were carriedout. ticks were previous where studies on andotherregions trict (studiedarea) Figure 1:GeographicallocalizationofSned locality, GafsaDis- (s.l.) lato sensu al., et 2015; (Nava group sanguineus R. Heki

N, 8° 47’ and and

E; mean altitude 313 altitude E; mean R. turanicus, R.

num. of ticks / of ticks num.

100 × (num. of infested sheep / 100 sheep ×(num. of infested these two species were pooled in were pooled in species two these

meters) (Figure

num. of infested sheep of infested num.

1). local The

num. of num. ------ratio M:F = ratio ticks n = (7%), and June May in (83%). only August collected were in few H. excavatum The s.l. was of sanguineus (6/8). R. peak sternum activity the The from Hyalomma whereas ears, the to attached ■ DISCUSSION and s.l. (n = Two sanguineus R. collected: were species tick = (p age group the to according September to April from intensities infestation between observed = (p October and July June, May, in adults in and September, and August April, in sheep young in observed was prevalence infestation ahigher although age group, to according prevalence infestation the between difference nificant = of (p males that than higher nificantly sig was of sheep female prevalence July,Except in infestation the (Table August in (3.7) intensity observed also was infestation maximum overall The (83%). August in maximal was prevalence infestation the whereas November March, and between observed was No infestation tick ■ RESULTS recorded in August: any control program should thus be applied applied be should thus program control any August: in recorded was prevalence infestation maximum study, the present the In , in (2011) Hyalomma (75.2%) impeltatum collected mainly sheep from al. et Bouhous hand, other al., et the 2004). On (Estrada-Peña Central North in sheep in species tick frequent most the as reported been has al., sanguineus 2004). study, However, R. present the in as et al., (Walker et tick 2003; sheep Estrada-Peña common most the is al., et 1999). turanicus (Bouattour R. tick summer s.l. a three-host is al., et (Rjeibi 2016b). District Kebili in R. reported sanguineusbeen 2015; Rjeibi al., et 2016a) Theileria transmits and al., et 1999; Rjeibi Tunisia al., et (Bouattour Southern and Central in present It mainly tick. is orthree-host a two- maybe H. excavatum al., et 2013; al., et 2016). (Estrada-Peña Domșa, species tick of other appearance the and disappearance their to lead therefore could e.g. Ixodes climate, arid the to not adapted are T South to subhumid) and (humid North alot from vary conditions mate Algeria). and ( Cli countries neighboring and Tunisian regions i tick-host (such other species dromedaries with as cohabitation tures, of pas nature systems, i.e. management the bioticabiotic factors, and both to related be may Tunisian areas different in sheep parasitizing Rhipicephalus by lowed out by Rjeibi et carried survey 0.7%) Another District. Kebili in excavatum H. that revealed (2016b)al. study, of present location the close the to District, Kebili in icasi 41.8%) (4.6%) areas; studied sanguineus all R. in and present were H. tum (Figure Saharan) and arid semiarid, K of Tunisia Ariana, (Jendouba, districts five in species of tick ence five excavatum R. sanguineus study: the in Two identified were species and guilhoni R. H. scupense, H. dromedarii, of H. marginatum, imens n the South), and to the introduction of infested animals from other other from animals of infested introduction South), the n the to and unisia (arid and Saharan). Several works show that some tick species species tick some show works that Several Saharan). (arid and unisia airouan, Kebili and Tataouine) in different bioclimatic zones (humid, (humid, zones bioclimatic Tataouine) and different Kebili in airouan,

dromedarii dromedarii

R. evertsi R. R. sanguineus s.l.313) (43.3%; sanguineus R. male than n= Hyalomma (n excavatum = (

( (three male and five female ticks). female five and male (three . In a similar survey, Rjeibi survey, (2015) al. et asimilar . In showed pres the to a lesser extent R. sanguineus extent alesser to

0.76). The same trend was observed for H. 0.76). observed was trend same The . R. cam R. and (7.8%) District, Tataouine in collected was September (TableSeptember

I). s pp. The variability among tick populations populations tick among variability pp. The was the most frequent tick in sheep, fol sheep, in tick frequent most the was

0.6). No significant differences were differences 0.6). No significant

8; 1.4%). Rhipicephalus

0.16).

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(45%), (45%), 1): turanicus R. ticks were mainly collected collected mainly were ticks

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Activité saisonnière des tiques infestant les ovins en Tunisie

Table I Monthly infestation indicators of sheep according to age and gender and monthly population dynamics of ticks according to their species in Tunisia

Indicators Oct. Nov. Dec. Jan. Feb. Mar. Apr. May Jun. Jul. Aug. Sep.

Num. infested Male 0/26 0/26 0/26 0/26 0/26 0/26 0/6 0/3 5/10 3/4 1/6 1/6 sheep / num. (50 ± 31) (75 ± 42) (17 ± 30) (17±30) examined Female 3/38 0/38 0/38 0/38 0/38 0/38 13/55 27/58 36/51 36/55 47/52 37/51 sheep (8 ± 9) (24 ± 11) (47 ± 13) (71 ± 13) (65 ± 13) (90 ± 8) (73 ± 12) (prevalence % and precision) Young 0/38 0/38 0/38 0/38 0/38 0/38 6/23 12/29 18/32 12/23 21/23 17/23 (26 ± 18) (41 ± 18) (56 ± 17) (52 ± 20) (91 ± 12) (74 ± 18) Adult 3/26 0/26 0/26 0/26 0/26 0/26 7/38 15/32 23/29 27/36 27/35 21/34 (12 ± 12) (18 ± 12) (47 ± 17) (79 ± 15) (75 ± 14) (77 ± 14) (62 ± 16) Overall 3/64 0/64 0/64 0/64 0/64 0/64 13/61 27/61 41/61 39/59 48/58 38/57 (5 ± 5) (21 ± 10) (44 ± 12) (67 ± 12) (66 ± 12) (83 ± 10) (67 ± 12)

Infestation Male 0 0 0 0 0 0 0 0 4 (20/5) 4 (12/3) 1 (1/1) 1 (1/1) intensity Female 1.3 (4/3) 0 0 0 0 0 1.5 1.7 2.6 2.5 3.8 2.6 (num. ticks / (19/13) (45/27) (93/36) (90/36) (178/47) (97/37) num. infested sheep) Young 0 0 0 0 0 0 1.7 1.6 2.7 2.5 3.2 (68/21) 2.2 (10/6) (19/12) (48/18) (30/12) (37/17) Adult 1.3 (4/3) 0 0 0 0 0 1.3 (9/7) 1.7 2.8 2.7 4.1 2.9 (26/15) (65/23) (72/27) (111/27) (61/21) Overall 1.3 (4/3) 0 0 0 0 0 1.5 1.7 2.8 2.6 3.7 2.6 (19/13) (45/27) (113/41) (102/39) (179/48) (98/38)

Total tick R. s. 4 0 0 0 0 0 19 39 112 102 179 97 number H. e. 00000006 1 0 0 1

Tick R. s. 3/64 0 0 0 0 0 13/61 27/61 41/61 39/59 48/58 38/57 infestation (5 ± 5) (21 ± 5) (44 ± 12) (67 ± 12) (66 ± 12) (83 ± 10) (67 ± 12) prevalence H. e. 0 0 0 0 0 0 0 4/61 1/61 0 0 1/57 = 100 x (7 ± 6) (2 ± 3) (2 ± 3) (num. sheep infested by tick sp. / num. examined sheep)

R. s.: Rhipicephalus sanguineus sensu lato; H. e: Hyalomma excavatum during this period. The tick infestation started in April and no infes- different: young sheep grazed near the farms with adults for a short tation was observed during the cold months (from November to period and were kept mostly inside. March) since the ticks were not active. Infestation onset is associated with the increase in temperature and photoperiod that promote the Although the number of examined males was often, by far, lower than development and activity of ticks (Dantas-Torres and Otranto, 2013). that of females, the results revealed that adult female sheep (except in Global warming projections for the study area show that infestations July) were more at risk than males, which were only infested between in the future may start much earlier in spring and/or late winter, June and September. The difference may be due to the fact that males which would extend the tick activity period. were often kept in the farm and had fewer grazing periods than females, as they were used for mating or fattening. Moreover, females There was no significant difference between the infestation preva- expressed immunodepression during pregnancy and lactation (Reh- lence in adult and young sheep, both groups being alternately most man et al., 2017). infested, which could be due to the monthly fluctuation of the exam- ined sample. This aleatory difference was unexpected because lambs The number of female ticks was higher than that of male for both R. are at first monogastric and do not graze, and thus release lower sanguineus s.l. and H. excavatum, but it was not significant for the latter. quantities of attractive gases for ticks (Bouattour et al., 1996). They Usually, the number of male ticks is higher because they spend a longer should thus be less infested than adults. Rjeibi et al. (2016b) also period attached to the animals, whereas female ticks engorge in more or observed no difference in the infestation prevalence between dif- less one week. This unusual observation could not be elucidated. ferent age groups, which could be because, in North Tunisia where The identification of attachment sites increases the efficiency of tick pastures are very rich, young sheep graze with adults. In Gafsa Dis- control, whether it is by tick removal or acaricide application (Gharbi trict, where our study was carried out, the management system was et al., 2013; Gharbi and Darghouth, 2014). 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Activité saisonnière des tiques infestant les ovins en Tunisie

Résumé Resumen Elati K., Ayadi A.A., Khamassi Khbou M., Jdidi M., Rekik M., Elati K., Ayadi A.A., Khamassi Khbou M., Jdidi M., Rekik M., Gharbi M. Dynamique des populations de tiques infestant les Gharbi M. Dinámica poblacional de garrapatas que infestan ovins dans les steppes arides de Tunisie ovejas en las estepas áridas de Túnez

Cette étude a cherché à déterminer la dynamique des popu- Este estudio tuvo como objetivo determinar la dinámica de la lations de tiques infestant les ovins dans la région de Gafsa población de garrapatas que infestan a las ovejas en la región (centre de la Tunisie). Les tiques ont été prélevées sur 57–64 de Gafsa (Túnez Central). Se recolectaron mensualmente moutons de race Barbarine choisis au hasard chaque mois pen- garrapatas al azar de 57–64 ovejas de raza Barbarina. Los ani- dant un an, d’octobre 2013 à septembre 2014. Au total, 560 males fueron monitoreados por un período de un año, desde tiques ont été collectées et identifiées. Elles appartenaient à octubre de 2013 hasta septiembre de 2014. Se recolectaron deux espèces : Rhipicephalus sanguineus sensu lato (98,6 %) e identificaron 560 garrapatas. Las garrapatas pertenecieron et Hyalomma excavatum (1,4 %). Les ovins n’ont été infestés a dos especies: Rhipicephalus sanguineus sensu lato (98,6%) que d’avril à octobre avec une prévalence maximale (nombre y Hyalomma excavatum (1,4%). Las ovejas sólo se infestaron d’animaux infestés / nombre d’animaux examinés) en août pour de abril a octubre con una prevalencia máxima de infestación R. sanguineus s.l. (83 %) et en mai pour H. excavatum (7 %). (número de animales infestados / número de animales exa- L’intensité d’infestation maximale (nombre de tiques / nombre minados) en agosto para R. sanguineus s.l. (83%), y en mayo d’animaux infestés) a été de 3,7 tiques par animal en août. Ces para H. excavatum (7%). La mayor intensidad de infestación données seront très utiles pour les éleveurs d’ovins et les vété- (número de garrapatas / número de ovejas infestadas) fue de rinaires pour mettre en place des mesures de lutte efficaces 3,7 en agosto. Estos resultados deberían ayudar a los propie- contre les tiques et les pathogènes qu’elles transmettent. tarios de ovejas y veterinarios a implementar programas de control eficientes contra las garrapatas y los patógenos que Mots-clés : ovin, Metastigmata, Rhipicephalus sanguineus transmiten. sensu lato, Hyalomma excavatum, dynamique des popula- tions, Tunisie Palabras clave: ovino, Metastigmata, Rhipicephalus sangui- neus sensu lato, Hyalomma excavatum, dinámica de pobla- ciones, Túnez Revue d’élevage et de médecine vétérinaire des pays tropicaux, 2018, 71 (3) : 131-135 des pays et de médecine vétérinaire Revue d’élevage 135