BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, researchlibraries, and research funders in the common goal of maximizing access to critical research.

Parasitism of Immature Stages of Haemaphysalis sulcata (Acari: Ixodidae) onSome Reptiles in TurkeyAuthor(s): Adem Keskin , Ahmet Bursali , Yusuf Kumlutas , Cetin Ilgaz , and Saban TekinSource: Journal of Parasitology, 99(5):752-755. 2013.Published By: American Society of ParasitologistsDOI: http://dx.doi.org/10.1645/13-187.1URL: http://www.bioone.org/doi/full/10.1645/13-187.1

BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, andenvironmental sciences. BioOne provides a sustainable online platform for over 170 journals and books publishedby nonprofit societies, associations, museums, institutions, and presses.

Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance ofBioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use.

Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiriesor rights and permissions requests should be directed to the individual publisher as copyright holder.

PARASITISM OF IMMATURE STAGES OF HAEMAPHYSALIS SULCATA (ACARI: IXODIDAE)

ON SOME REPTILES IN TURKEY

Adem Keskin, Ahmet Bursali, Yusuf Kumlutas*, Cetin Ilgaz*, and Saban Tekin†

Department of Biology, Gaziosmanpasa University, Faculty of Science & Art, 60250, Tasliciftlik, Tokat, Turkey. Correspondence should be sent to:bursali383@yahoo.com

ABSTRACT: Reptiles may contribute to maintaining tick populations by feeding larvae, nymphs, and adults. The life cycles and tick–host associations of many Turkish ticks are still poorly known, and only 3 ixodid tick species have been reported on 7 reptile species inTurkey. In this study, we performed a tick survey on reptiles in the Southeastern Anatolia Region of Turkey. In 2005, 57 reptiles (52lizards and 5 snakes) comprising 10 species from 5 families were captured and examined for tick infestation. A total of 427 ticks wascollected. The majority of ticks found on lizards was the immature stages ofHaemaphysalis sulcata, 420 larvae and 4 nymphs. The onlyadult ticks recorded on the agamid lizard, Laudakia stellio, were Hyalomma aegyptium (1?, 2 /). The highest tick infestation rate wasrecorded on specimens of Timon princeps. This study is the first detailed investigation on ticks infesting reptiles in Turkey. To the bestof our knowledge, these tick–host associations have never been documented in the literature.

Hosts of ticks (Acari: Ixodida), especially small vertebrates,

serve as reservoirs for many pathogenic organisms, and play an

important role for the transmission of several pathogenic

organisms to animals and humans. Tick infestations of domestic

animals are well studied (Sayin and Dumanli, 1982; Ica et al.,

2007; Bakirci et al., 2012) in Turkey. On the contrary, ticks

infesting small vertebrates such as birds, rodents, and reptiles

have been generally neglected.

Adults of Haemaphysalis sulcata are active during the cold

season, whereas the immature stages are active during the summer

(Estrada-Pena et al., 2004). Large mammals including cattle and

sheep are the major hosts for the adults of H. sulcata, whereas

reptiles and birds are hosts for the immature ones. Haemphysalis

sulcata is an economically important tick species, since it may

transmit several pathogenic organisms belong to the genera

Babesia and Theileria (Hoogstraal et al., 1981; Kolonin, 2009).

This tick also transmits Anaplasma ovis, which causes ovine

anaplasmosis (Walker et al., 2003; Estrada-Pena et al., 2004).

Haemaphysalis sulcata has been found throughout Turkey and

neighboring countries (Merdivenci, 1969; Kolonin, 2009; Bursali

et al., 2012). However, to date, no studies have been performed to

determine the life cycle, host association, reservoir status, and

vectorial capacity of H. sulcata in Turkey. In a recent study, the

presence of Anaplasma phagocytophilum in H. sulcata was

reported in Turkey; however, it is not known whether it is a

vector or reservoir for A. phagocytophilum (Aktas et al., 2012).

In this study, we provide quantitative ecological information on

relationships between H. sulcata and its reptilian hosts in Turkey.

To our knowledge, this is the first systematic study on ticks

infesting reptiles in Turkey.

MATERIALS AND METHODS

Study areas

Turkey consists of 7 geographical regions; Marmara, Aegean, BlackSea, Central Anatolia, Eastern Anatolia, Southeastern Anatolia, and theMediterranean. The study area, Southeastern Anatolia region, is located

in the southeastern part of the Anatolian peninsula of Turkey (Fig. 1) andhas 2 subregions, Middle Euphrates and Tigris. This region has an area of57,000 km2 and altitudes range from 800 to 1,000 m. The mean annualprecipitation is 620.6 mm. The mean annual maximum temperature is 20.1C, whereas the mean minimum annual temperature is 4.2 C (Unal et al.,2003). The Southeastern Anatolia Region has a semiarid continentalclimate, and primary vegetation type is steppe. The summers are very hotand dry, whereas winters are cold and often snowy. Small ruminants arethe main domestic stocks, but there is also a small amount of cattlehusbandry. Wild animals such as small mammals and ground-feedingbirds are very common in this region. This region constitutes one of therichest regions of Turkey in terms of lizard and snake species (Baran andAtatur, 1998; Sindaco et al., 2000).

Trapping and identification of reptiles

Reptiles were captured by hand and transferred to the laboratory incotton bags. The specimens were fixed with 5% formaldehyde in 70%ethanol and then preserved in 70% ethanol according to the methoddescribed by Basoglu and Baran (1977, 1980). The specimens weredeposited in the herpetological collection of the Fauna and FloraResearch and Application Center, Dokuz Eylul University, Izmir, Turkey.Identification of reptile specimens collected from Southeastern Anatoliautilized the available published literature (Basoglu and Baran, 1977, 1980;Leviton et al., 1992; Baran and Atatur, 1998; Sindaco et al., 2000).

Collection and identification of ticks

Ticks were removed from the lizard and snake skins with the help oftweezers. All of the tick specimens were stored in 70% alcohol. Fortaxonomic identification, tick samples were sent to the Turkish TickCollection (TTC), Department of Biology, Gaziosmanpasa University,Tokat, Turkey. Ticks were identified on the basis of morphologicalcharacters of Nosek and Sixl (1972) and Filippova (1997) and deposited inthe TTC with accession numbers (Table I).

RESULTS

Species composition of reptiles

Overall, 57 reptile specimens (5 snakes and 52 lizards) from 5

families and belonging to 10 species were examined for tick

infestation from 9 different localities of the Southeastern Anatolia

region (Table I). Reptile specimens infested by the ticks were

identified as Laudakia stellio (Agamidae), Apathya cappadocica,

Lacerta media, Ophisops elegans, Timon princeps (Lacertidae),

Eumeces schneideri, Trachylepis aurata (Scincidae), and Myrioph-

olis macrorhyncha (Leptotyphlopidae). There was no tick

infestation on 2 reptilian species, Varanus griseus (Varanidae)

and Chalcides ocellatus (Scincidae). Within the examined reptiles,

the most common reptilian species were identified as O. elegans

and Timon aurata, whereas E. schneideri and L. media were

Received 15 January 2013; revised 21 March 2013; accepted 2 April2013.

* Department of Biology, Dokuz Eylul University, Faculty of Science,35160, Buca, Izmir, Turkey.

† Department of Molecular Biology and Genetics, GaziosmanpasaUniversity, Faculty of Science & Art, 60250, Tasliciftlik, Tokat,Turkey.

DOI: 10.1645/13-187.1

J. Parasitol., 99(5), 2013, pp. 752–755

� American Society of Parasitologists 2013

752

represented by a single specimen. Most of the examined reptiles

were captured in Batman-Hasankeyf and Diyarbakir-Cungus

localities.

Ticks infested on reptiles and attachment sites

In the present study, a total 427 ticks was collected from 57

reptiles. Almost all of the ticks collected from reptiles were

identified as H. sulcata (420 larvae, 4 nymphs) on the basis of

morphological characters. Larvae and nymphs of the ticks can

easily be distinguished from those of other immature haemaphy-

salids by a combination of the following characters: palps conical,

palpal segment II without caudal spur, basis capituli rectangular,

and coxae without spurs. The most severe tick infestation was

recorded on the specimens of T. princeps. Larval H. sulcata were

mainly found on the lizard’s necks, behind the ear, or axillae of

the forelegs and hind legs, whereas only several larval specimens

were found between the fingers of hind legs. Nymphs were found

only behind the ear and on the hind legs. A larval form of H.

sulcata was found on the neck of M. macrorhyncha, a snake

species examined in this study. The highest infestation of H.

sulcata was recorded on T. princeps, whereas the lowest was

reported on E. schneideri, M. macrorhyncha, and O. elegans. In

addition, only 3 adults ofHyalomma aegyptium were found on the

axilla of the forelegs of an agamid lizard, Laudakia stellio.

DISCUSSION

Worldwide, most of the papers about tick infestations of wild

animals have been associated with birds or small rodents

(Hoogstraal et al., 1961, 1963; Guglielmone and Nava, 2010;

Saraiva et al., 2012), and reptilian hosts of the ticks have been

frequently disregarded. However, reptiles may serve as a suitable

host for various tick species (Filippova, 1997; Durden et al., 2002;

Durden and Knapp, 2005) and contribute to transmission of

pathogenic organisms (Clark et al., 2005; Dsouli et al., 2006).

Therefore, reptilian hosts of the ticks must be identified to

elucidate the natural cycles of pathogenic organisms transmitted

by the ticks. However, although there have been several studies on

medical and veterinary importance of ticks in Turkey (Sayin and

Dumanli, 1982; Ica et al., 2007; Bakirci et al., 2012; Aktas et al.,

2012), ecological and systematic studies on ticks have been mainly

neglected. Moreover, life cycles and tick–host association of many

Turkish ticks are still poorly known, even though Turkey has very

rich reptile fauna (Baran and Atatur, 1998; Sindaco et al., 2000).

To date, only 3 tick species have been reported from 7 reptile

species (Hoogstraal, 1959; Bursali et al., 2012; Keskin et al.,

2012).

In earlier studies, A. cappadocica, L. stellio, and O. elegans have

been found as reptilian hosts of Haemaphysalis sulcata (Hoog-

straal, 1959). Similarly, Hyalomma aegyptium was documented on

L. stellio and Testudo graeca (Hoogstraal and Kaiser, 1960;

Bursali et al., 2012). Recently, Keskin et al. (2012) also reported 2

lizards, Lacerta media and Darevskia rudis, as the hosts of Ixodes

ricinus. The main objective of present study is to provide

biological and ecological data on Turkish Haemaphysalis sulcata

and to reveal its natural reptilian hosts. Hence, the results of the

present study are very important to understand the ecology and

host association of H. sulcata in Turkey.

In the present study, we collected H. sulcata from 10 different

reptile species from the Southeastern Anatolia region of Turkey.

Trachylepis aurata and O. elegans were the lizard species most

commonly captured in this study, but the highest tick infestation

was recorded on Timon princeps. Similar high tick infestation

rates were reported in other reptiles by several authors (Durden et

al., 2002; Durden and Knapp, 2005). This is the first report of H.

sulcata infestation on T. princeps, and it seems that T. princeps is

the main reptilian host of the immature H. sulcata in the

Southeastern Anatolia region of Turkey. The lizard lives in

northwestern Iran, northeastern Iraq, and Southeastern Anatolia,

where it is found in rocky areas in open oak woodland and

scrubland, and sometimes in open grassland (Ilgaz and Kumlutas,

2008).

The infestations of H. sulcata on L. media and Trachylepis

aurata have also been documented for the first time in this study.

However, infestation rates on these 2 reptiles were lower than

Timon princeps. In addition, a single H. sulcata larva was found

on the only snake species, M. macrorhyncha, examined in this

study. It is clear that further studies should be conducted to

determine the tick species infesting other reptile species and their

FIGURE 1. Map of research area,Southeastern Anatolia region in Tur-key.

KESKIN ET AL.—TICKS INFESTING REPTILES 753

potential for transmitting tick-borne pathogens to humans and

animals.

LITERATURE CITED

AKTAS, M., K. ALTAY, S. OZUBEK, AND N. DUMANLI. 2012. A survey ofixodid ticks feeding on cattle and prevalence of tick-borne pathogensin the Black Sea region of Turkey. Veterinary Parasitology 187: 567–571.

BAKIRCI, S., H. SARALI, L. AYDIN, H. EREN, AND T. KARAGENC. 2012.Distribution and seasonal activity of tick species on cattle in the WestAegean region of Turkey. Experimental and Applied Acarology 56:

165–178.BARAN, I., AND M. K. ATATUR. 1998. The herpetofauna of Turkey

(amphibians and reptiles). Republic of Turkey, Ministry of theEnvironment, Ankara, 214 p.

BASOGLU, M., AND I. BARAN. 1977. Turkiye Surungenleri Kisim I.Kaplumbaga ve Kertenkeleler. Ege Universitesi Fen FakultesiKitaplar Serisi, Izmir. 272 p.

——— AND ———. 1980. Turkiye Surungenleri Kisim II. Ege UniversitesiFen Fakultesi Kitaplar Serisi, Izmir, 218 p.

BURSALI, A., A. KESKIN, AND S. TEKIN. 2012. A review of the ticks (Acari:Ixodida) of Turkey: Species diversity, hosts and geographicaldistribution. Experimental and Applied Acarology 57: 91–104.

CLARK, K., A. HENDRICKS, AND D. BURGE. 2005. Molecular identificationand analysis of Borrelia burgdorferi sensu lato in lizards in thesoutheastern United States. Applied and Environmental Microbiol-ogy 71: 2616–2625.

DSOULI, N., H. YOUSNSI-KABACHII, D. POSTIC, S. NOUIRA, L. GERN, AND A.BOUATTOUR. 2006. Reservoir role of lizard Psammodromuas algirus intransmission cycle of Borrelia burgdorferi sensu lato (Spirochaetace-ae) in Tunisia. Journal of Medical Entomology 43: 737–742.

DURDEN, L. A., AND C. R. KNAPP. 2005. Ticks parasitizing reptiles in theBahamas. Journal of Medical and Veterinary Entomology 19: 326–328.

———, J. H. OLIVER JR., C. W. BANKS, AND G. N. VOGEL. 2002.Parasitism of lizards by immature stages of the blacklegged tick,Ixodes scapularis (Acari, Ixodidae). Experimental and AppliedAcarology 26: 257–266.

ESTRADA-PENA, A., A. BOUATTOUR, J. L. CAMICAS, AND A. R. WALKER.2004. Ticks of veterinary and medical importance: The Mediterra-nean Basin. A guide of identification of species. University ofZaragoza Press, Zaragoza, Spain, 131 p.

FILIPPOVA, N. A. 1997. Ixodid ticks of subfamily Amblyomminae. InFauna of Russia and neighbouring countries, vol. 4, no. 5. NaukaPublishing House, St. Petersburg, Russia, 436 p.

GUGLIELMONE, A. A., AND S. NAVA. 2010. Rodents of the subfamilyCaviinae (Hystricognathi, Caviidae) as hosts for hard ticks (Acari:Ixodidae). Mastozoologıa Neotropical 17: 279–286.

HOOGSTRAAL, H. 1959. Biological observations on certain TurkishHaemaphysalis ticks (Ixodoidea, Ixodidae). Journal of Parasitology45: 227–232.

———, AND M. N. KAISER. 1960. Some host relationships of the Tortoisetick, Hyalomma (Hyalommasta) aegyptium (L.) (Ixodoidea: Ixodi-dae) in Turkey. Annals of the Entomological Society of America 53:

457–458.———, ———, M. A. TRAYLOR, S. A. GABER, AND E. GUINDY. 1961.

Ticks (Ixodoidea) on birds migrating from Africa to Europe andAsia. Bulletin of the World Health Organization 24: 197–212.

———, ———, ———, E. GUINDY, AND S. A. GABER. 1963. Ticks(Ixodidae) on birds migrating from Europe and Asia to Africa, 1959–61. Bulletin of the World Health Organization 28: 235–262.

———, H. Y. WASSEF, AND W. BUTTIKER. 1981. Ticks (Acarina) of SaudiArabia. Fam. Argasidae, Ixodidae. Fauna of Saudi Arabia 3: 25–110.

ICA, A., A. INCI, Z. VATANSEVER, AND Z. KARAER. 2007. Status of tickinfestation of cattle in the Kayseri region of Turkey. ParasitologyResearch 101(Suppl. 2): S167–S169.

ILGAZ, C., AND Y. KUMLUTAS. 2008. The morphology and distribution ofTimon princeps (Blanford, 1874) (Sauria: Lacertidae) in SoutheasternAnatolia, Turkey. North-Western Journal of Zoology 4: 247–262.

KESKIN, A., E. SIMSEK, AND A. BURSALI. 2012. Two new host data forIxodes ricinus (Acari: Ixodidae); Lacerta media and Lacerta rudisT

ABLEI.LocationofcollectionandreptilianhostsofHaem

aphysalissulcata

intheSoutheasternAnatoliaregionin

Turkey.

Host

species

Family

Number

of

examined

lizards

Locality

Date

Tickspecies

Stage

Accessionno.

Apathyacappadocica

Lacertidae

7Diyarbakir-C

ermik

11June2005

Haem

aphysalissulcata

4L

TTC-151

Chalcides

ocellatus

Scincidae

4Gaziantep-Sahinbey

23April2005

Eumeces

schneideri

Scincidae

1Diyarbakir-C

ungus

11June2005

Haem

aphysalissulcata

1N

TTC-152

Lacertamedia*

Lacertidae

1Siirt-Eruh

14June2005

Haem

aphysalissulcata

28L

TTC-153

Laudakia

stellio

Agamidae

2Diyarbakir-C

ermik

11June2005

Laudakia

stellio

Agamidae

1Diyarbakir-Siverek

30April2005

Hyalommaaegyptium

1?,2

/TTC-154

Myriopholismacrorhyncha*

Leptotyphlopidae

1Batm

an-H

asankeyf

13June2005

Haem

aphysalissulcata

1L

TTC-155

Myriopholismacrorhyncha

Leptotyphlopidae

4Adıyaman-Sambayat

8June2005

Ophisopselegans

Lacertidae

1Sanliurfa-C

eylanpinar

28April2005

Ophisopselegans

Lacertidae

13

Diyarbakir-C

ungus

11June2005

Haem

aphysalissulcata

1N

TTC-156

Tim

onprinceps*

Lacertidae

6Siirt-Eruh

14June2005

Haem

aphysalissulcata

368L,2N

TTC-157

Trachylepisaurata*

Scincidae

13

Batm

an-H

asankeyf

13June2005

Haem

aphysalissulcata

21L

TTC-158

Trachylepisaurata

Scincidae

1Kilis

23April2005

Varanusgriseus

Varanidae

2Sanliurfa-C

eylanpinar

28April2005

Total

57

427

L:larva,N:nymph.

*New

tick–host

association.

754 THE JOURNAL OF PARASITOLOGY, VOL. 99, NO. 5, OCTOBER 2013

(Diapsida: Lacertidae). 21. Proceedings of the National BiologyCongress, Izmir, Turkey, p. 1021.

KOLONIN, G. V. 2009. Fauna of ixodid ticks of the world (Acari: Ixodidae).http://www.kolonin.org/18_1.html. Accessed 12 December 2012.

LEVITON, A. E., S. C. ANDERSON, K. ADLER, AND S. A. MINTON. 1992.Handbook to Middle East amphibians and reptiles. Contributions toHerpetology 8. Society for the Study of Amphibians and Reptiles,Oxford, Ohio, 252 p.

MERDIVENCI, A. 1969. Turkiye keneleri uzerine arastırmalar. KurtulusMatbaası. Istanbul, 420 p.

NOSEK, J., AND W. SIXL 1972. Central-European ticks (Ixodidae). Key fordetermination. Mitteilungen der Abteilung fur Zoologic am Land-esmuseum Joanneum 1: 61–92.

SARAIVA, D. G., G. F. FOURNIER, T. F. MARTINS, K. P. LEAL, F. N. VIEIRA,E. M. CAMARA, C. G. COSTA, V. C. ONOFRIO, D. M. BARROS-BATTESTI,A. A. GUGLIELMONE ET AL. 2012. Ticks (Acari: Ixodidae) associated

with small terrestrial mammals in the state of Minas Gerais,southeastern Brazil. Experimental and Applied Acarology 58: 159–166.

SAYIN, F., AND N. DUMANLI. 1982. Elazıg bolgesinde evcil hayvanlardagorulen kene (Ixodoidea) turleri ile ilgili epizootiyolojik arastırmalar.Veterinary Journal of Ankara University 29: 344–362.

SINDACO, R., A.VENCHI, G. M. CARPANETO, AND M. A. BOLOGNA. 2000.The reptiles of Anatolia: A checklist and zoogeographical analysis.Biogeographia 21: 441–554.

UNAL, Y, T. KINDAP, AND M. KARACA. 2003. Redefining the climate zonesof Turkey using cluster analysis. International Journal of Climatol-ogy 23: 1045–1055.

WALKER, A. R., A. BOUATTOUR, J. L. CAMICAS, A. ESTRADA-PENA, I. G.HORAK, A. LATIF, R. G. PEGRAM, AND P. M. PRESTON. 2003. Ticks ofdomestic animals in Africa: A guide to identification of species.Biosience Reports, Edinburgh. U.K., p. 221.

KESKIN ET AL.—TICKS INFESTING REPTILES 755