(Mer - , 1820), along the Bulgarian Black sea coast: a compilation … · 2019-03-01 · 1 93). th...

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220 sHOrt NOte HerPetOzOa 31 (3/4) Wien, 28. Februar 2019 sHOrt NOte skin glands contain poisons, as seen also in leptodactylids (Prates et al. 2012). thus, it may well be that beside the size of the prey, the death of the juvenile viper was caused by the frog’s potentially toxic secretions. the prey type and size of the snake could indicate that juvenile C. d. ruruima are dietary generalists. Moreover, the authors recorded here for the first time an amphib- ian as prey of C. d. ruruima. aCKNOWLeDGMeNts: the authors are grateful to Priscila azarak (Laboratório de evolução e Genética animal, Universidade Federal do amazonas - LeGaL/UFaM) who identified the frog species. reFereNCes: CLarK, r. W. (2004): timber rattlesnakes (Crotalus horridus) use chemical cues to select ambush sites.- Journal of Chemical ecology, Ithaca, New York; 30 (3): 607-617. HOGe, a. r. (1965): Preliminary account on neotropical Crotalinae (serpentes: Viperidae).- Memórias do Instituto Butan - tan, são Paulo; 32: 109-184. KLaUBer L. M. (1972): rattlesnakes. their habits, life histories and influence on mankind. second edition. Berkeley (University of California Press), pp. 1536. NasCIMeNtO, s. P. & NOrONHa, M. D. N. & MUNIz, e. G. & LóPez-LOzaNO, J. L. & aLVes-GOMes, J. a. (2007): Característica epi- demiológica e clínica dos acidentes por serpentes peçonhentas no estado de roraima, Brasil.- Mens agitat / academia roraimense de Ciências, Boa Vista; 2 (2): 43-54. Prates, I. & aNtONIazzI, M. M. & sCIaNI, J. M. & PIMeNta, D. C. & tOLeDO, L. F. & HaDDaD, C. F. & JareD, C. (2012): skin glands, poi- son and mimicry in dendrobatid and leptodactylid amphibians.- Journal of Morphology, Malden, etc.; 273 (3): 279-290. sazIMa, I. & MartINs, M. (1990): Presas grandes e serpentes jovens: Quando os olhos são maiores que a boca.- Memórias do Instituto Butantan, são Paulo; 52 (3): 73-79. V azOLINI, P. e. & raMOs-COsta, a. M. & VItt, L. J. (1980): rép teis das Caatingas. rio de Janeiro (academia Brasileira de Ciências), pp. 161. KeY WOrDs: reptilia: squamata: serpentes: Viperidae: Crotalus durissus ruruima; feeding ecology, prey, veterinary medicine sUBMItteD: February 17, 2018 aUtHOrs: anderson Maciel rOCHa (Corre- sponding author < [email protected] >) 1) ; Cleuner PareNte De FreItas 1) & Patrik F. VIaNa 2, 3) 1) Faculdade Cathedral de ensino superior, Faculdade Cathedral, Laboratório de zoologia apli- cada de Vertebrados terrestres e aquáticos, avenida Luis Canuto Chaves, 293, Caçari, CeP 69307-655, Boa Vista, rr, Brasil 2) Laboratory of animal Genetics, Instituto Nacional de Pesquisas da amazônia - Campus II, av. andré araújo, 2936, 69080-971 Manaus, aM, Brazil. 3) Programa de Pós-Graduação em Genética Conservação e Biologia evolutiva, Instituto Nacional de Pesquisas da amazônia - Campus II, av. andré araújo, 2936, 69080-971 Manaus, aM, Brazil. Xerotyphlops vermicularis (Mer - reM, 1820), along the Bulgarian Black sea coast: a compilation of new and published records the eurasian Blind snake, Xero - typhlops vermicularis (MerreM, 1820), the only representative of the snake family typhlopidae (superfamily scolecophidia) in europe (GrILLItsCH & GrILLItsCH 1993), is found in the southern parts of the Balkan Peninsula (GrILLItsCH & GrILLItsCH 1993; sILLerO et al. 2014). the snake represents an element of the turano-Mediterranean chorotype (MIzseI et al. 2017), in which all populations in the Balkans probably origi- nate from eastern anatolian ancestors (KOr - NILIOs 2017). the eurasian Blind snake prefers xerothermic habitats with deep, dry and soft (sandy) soil where it can burrow, typically rocky slopes with low, sparse bush vegetation, open areas with stones as well as cultivated fields (GrIL LItsCH & GrILLItsCH 1993). the northeastern edge of the snake’s distribution in the Balkans runs through Bulgaria (see BesH KOV & NaNeV 2006; stOJaNOV et al. 2011), where it occurs scat- tered at altitudes below 500 m a.s.l. in the southern parts of the country, along the warm valleys of the struma river (sW Bulgaria), the lower Maritsa river (Harmanli region), the arda river (eastern rhodope Mts.) and the tundja river (Derventski Heights, se Bulgaria; Fig. 1a), in which the Mediterra- nean climatic influence is strongest (BesH - KOV 1998; stOJaNOV et al. 2011). after more than 100 years, the species was redis- covered in the western rhodope Mts. (JaBLONsKI & BaLeJ 2015). Besides, there are historical, no longer confirmed records of X. vermicularis from isolated localities southeast of Burgas city (Black sea coast, eastern slopes of strandzha Mts. (see stOJaNOV et al. 2011). to compile the knowledge of records of this species along the Bulgarian Black sea coast, the authors of the present note reviewed the available literature (BUresH & zONKOV 1934; BesHKOV 1956, 1961, 1985; P aPsDOrF 1971; BartOsIK 1981; KüHNeMaNN 1981; BUseKe 1982; tHIeMe 1986; ČIHař 1989; GrILLItsCH & GrILLItsCH 1993; stO - JaNOV et al. 2011) and added their unpub-

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220 sHOrt NOte HerPetOzOa 31 (3/4) Wien, 28. Februar 2019 sHOrt NOte

skin glands contain poisons, as seen also inleptodactylids (Prates et al. 2012). thus, itmay well be that beside the size of the prey,the death of the juvenile viper was causedby the frog’s potentially toxic secretions.the prey type and size of the snake couldindicate that juvenile C. d. ruruima aredietary generalists. Moreover, the authorsrecorded here for the first time an amphib-ian as prey of C. d. ruruima.

aCKNOWLeDGMeNts: the authors aregrateful to Priscila azarak (Laboratório de evoluçãoe Genética animal, Universidade Federal doamazonas - LeGaL/UFaM) who identified the frogspecies.

reFereNCes: CLarK, r. W. (2004): timberrattlesnakes (Crotalus horridus) use chemical cues toselect ambush sites.- Journal of Chemical ecology,Ithaca, New York; 30 (3): 607-617. HOGe, a. r.(1965): Preliminary account on neotropical Crotalinae(serpentes: Viperidae).- Memórias do Instituto Butan -tan, são Paulo; 32: 109-184. KLaUBer L. M. (1972):rattlesnakes. their habits, life histories and influenceon mankind. second edition. Berkeley (University ofCalifornia Press), pp. 1536. NasCIMeNtO, s. P. &NOrONHa, M. D. N. & MUNIz, e. G. & LóPez-LOzaNO,J. L. & aLVes-GOMes, J. a. (2007): Característica epi-demiológica e clínica dos acidentes por serpentespeçonhentas no estado de roraima, Brasil.- Mensagitat / academia roraimense de Ciências, Boa Vista;2 (2): 43-54. Prates, I. & aNtONIazzI, M. M. &sCIaNI, J. M. & PIMeNta, D. C. & tOLeDO, L. F. &HaDDaD, C. F. & JareD, C. (2012): skin glands, poi-son and mimicry in dendrobatid and leptodactylidamphibians.- Journal of Morphology, Malden, etc.;273 (3): 279-290. sazIMa, I. & MartINs, M. (1990):Presas grandes e serpentes jovens: Quando os olhossão maiores que a boca.- Memórias do InstitutoButantan, são Paulo; 52 (3): 73-79. VazOLINI, P. e. &raMOs-COsta, a. M. & VItt, L. J. (1980): rép teis dasCaatingas. rio de Janeiro (academia Brasileira deCiências), pp. 161.

KeY WOrDs: reptilia: squamata: serpentes:Viperidae: Crotalus durissus ruruima; feeding ecology,prey, veterinary medicine

sUBMItteD: February 17, 2018

aUtHOrs: anderson Maciel rOCHa (Corre -sponding author < [email protected] >) 1); CleunerPareNte De FreItas 1) & Patrik F. VIaNa 2, 3)

1) Faculdade Cathedral de ensino superior,Faculdade Cathedral, Laboratório de zoologia apli -cada de Vertebrados terrestres e aquáticos, avenidaLuis Canuto Chaves, 293, Caçari, CeP 69307-655, BoaVista, rr, Brasil

2) Laboratory of animal Genetics, InstitutoNacional de Pesquisas da amazônia - Campus II, av.andré araújo, 2936, 69080-971 Manaus, aM, Brazil.

3) Programa de Pós-Graduação em GenéticaConservação e Biologia evolutiva, Instituto Nacionalde Pesquisas da amazônia - Campus II, av. andréaraújo, 2936, 69080-971 Manaus, aM, Brazil.

Xerotyphlops vermicularis (Mer -reM, 1820), along the Bulgarian

Black sea coast: a compilation ofnew and published records

the eurasian Blind snake, Xero -typhlops vermicularis (MerreM, 1820), theonly representative of the snake familytyphlopidae (superfamily scolecophidia) ineurope (GrILLItsCH & GrILLItsCH 1993), isfound in the southern parts of the BalkanPeninsula (GrILLItsCH & GrILLItsCH 1993;sILLerO et al. 2014). the snake representsan element of the turano-Mediterraneanchorotype (MIzseI et al. 2017), in which allpopulations in the Balkans probably origi-nate from eastern anatolian ancestors (KOr -NILIOs 2017). the eurasian Blind snakeprefers xerothermic habitats with deep, dryand soft (sandy) soil where it can burrow,typically rocky slopes with low, sparse bushvegetation, open areas with stones as well ascultivated fields (GrIL LItsCH & GrILLItsCH1993). the northeastern edge of the snake’sdistribution in the Balkans runs throughBulgaria (see BesH KOV & NaNeV 2006;stOJaNOV et al. 2011), where it occurs scat-tered at altitudes below 500 m a.s.l. in thesouthern parts of the country, along the warmvalleys of the struma river (sW Bulgaria),the lower Maritsa river (Harmanli region),the arda river (eastern rhodope Mts.) andthe tundja river (Derventski Heights, seBulgaria; Fig. 1a), in which the Mediterra -nean climatic influence is strongest (BesH -KOV 1998; stOJaNOV et al. 2011). aftermore than 100 years, the species was redis-covered in the western rhodope Mts.(JaBLONsKI & BaLeJ 2015). Besides, thereare historical, no longer confirmed recordsof X. vermicularis from isolated localitiessoutheast of Burgas city (Black sea coast,eastern slopes of strandzha Mts. (seestOJaNOV et al. 2011).

to compile the knowledge of recordsof this species along the Bulgarian Blacksea coast, the authors of the present notereviewed the available literature (BUresH &zONKOV 1934; BesHKOV 1956, 1961, 1985;PaPsDOrF 1971; BartOsIK 1981; KüHNeMaNN1981; BUseKe 1982; tHIeMe 1986; ČIHař1989; GrILLItsCH & GrILLItsCH 1993; stO -JaNOV et al. 2011) and added their unpub-

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lished data and recent observations fromseveral field excursions. Coordinates as -signed to some historical records corre-spond to assumed closest named places andthus, are not accurate (table 1).

Fifteen different observations of X.vermicularis, reporting more than 30 ob -served individuals, were published between1934 and 1989 (for references see table 1).all these observations were made in theperiod of May until august, from mainlystony and sandy habitats, at altitudes rang-ing from 0 to 100 m a. s. l. Most records arefrom Cape “Maslen Nos” (five records be -tween 1954 and 1957) and arkutino (fourrecords, 1976–1980). Interestingly, the north -ernmost record originates from an island(sveti Ivan) located 1 km off the coast; thesouthernost is from a small valley betweenthe town of ahtopol and the Veleka river(Fig. 1). Moreover, the authors add threerecent records obtained during field studies:one adult individual observed near Pri -morsko town (observed by Nikolay tzaN -KOV) in June 2009; two adults and one juve-nile found near arkutino (observed byandrei stOJaNOV) in March 2010; and oneadult, not far from the second record locali-ty (observed by thomas reICH), in June2017 (Fig. 2). all individuals of these re -cent records were found under stones in theimmediate environs of two unfinished andabandoned hotel complexes ‟Perla 2” and‟zname Na Mira”. Overall, 18 records of X.vermicularis are known from the BulgarianBlack sea coast to date.

the record localities, which are clos-est to the Black sea records, are situatedalong the tundzha river (Lesovo village,Derventski Heights - stOeV 2000; stOJa -NOV et al. 2001), approximately 100 km up -country (Fig. 1a). Between the tundzhariver valley and the Black sea coast popu-lations there are agricultural fields and thewooded areas of the strandzha Mts., whichboth lack suitable habitats for the species.the authors hypothesize that these two pop-ulations are currently isolated from eachother; however, additional field research isnecessary to verify this assumption. Bothpopulations are probably remnants of ana -tolian colonization waves that propagatedalong the Black sea coast during the Holo -cene. the closest known localities in tur -

key lie in the vicinity of Istanbul, approxi-mately 160 km in a southeastern direction.No recent records are known from the Blacksea coast of european turkey (JaBLONsKI &stLOUKaL 2012; aFsar et al. 2016), al -though, a model of the potential distributionof X. vermicularis in turkey (aFsar et al.2016) roughly identified the whole euro -pean part of this country as a suitable habi-tat for this species.

Based on the published records, theBulgarian Black sea Xerotyphlops are cur-rently isolated from the neighboring popula-tions in Bulgaria and turkey. a similar dis-tribution has been observed in the snakespecies Platyceps collaris (MüLLer, 1878),and Zamenis situla (LINNaeUs, 1758), whichare missing in some Black sea regions ofeuropean turkey but found in southeast Bul -garia between ahtopol and Burgas or intheir close vicinity (stOJaNOV et al. 2011;sINDaCO et al. 2013). In the light of its iso-lated occurrence near the Bulgarian Blacksea coast, one cannot exclude accidental in -troduction of X. vermicularis (e. g., fromGreece) along with soils and building mate-rials, in ancient times. as is known, ancienttowns such as sozopol or ahtopol hadstrong commercial and cultural relations tocities of ancient Greece. a similar patternof accidental historical introduction fromGreek territory to other Mediterranean areaswas described for Chalcides ocellatus(FOrsKåL, 1775) (KOrNILIOs et al. 2010).

If the theory of unintentional anthro-pogenic introduction (e.g., from ancientGreece) is discarded, the present occurrenceof X. vermicularis along the Bulgarian Blacksea coast is most likely the result of discon-tinuous peripheral shrinkage of its oncewider and continuous range that had estab-lished before the formation of the Bosphorusstrait, more than 11,000 ybp (KereY et al.2004). this explanation is supported by twofacts: (i) the southwestern Black sea coastalarea was less wooded than now (OraCHeV2012) and, thus more suitable for X. vermic-ularis, and (ii) the Island of sveti Ivan nearsozopol, record locality of X. vermicularis,can have been colonized in a natural waysince the island was connected to the main-land until 6,000 ybp (when the coastline wasat least 10 m lower than today; see FILIPOVa-MarINOVa et al. 2011).

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222 sHOrt NOte HerPetOzOa 31 (3/4) Wien, 28. Februar 2019 sHOrt NOte

Fig. 1: Distribution map of published and new record localities of Xerotyphlops vermicularis (MerreM, 1820),along the Bulgarian Black sea coast (for details see corresponding numbers in table 1). a – Inset showing the

current distribution of the species in Bulgaria based on stOJaNOV et al. (2001). the position of map B is shown; B – records along the Bulgarian Black sea coast; C – Inset showing details of the area north of arkutino.

Fig. 2: a – the individual of Xerotyphlops vermicularis (MerreM, 1820), recorded near arkutino in June 2017; B – the place of the finding. Photos thomas reICH.

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sHOrt NOte HerPetOzOa 31 (3/4) Wien, 28. Februar 2019 sHOrt NOte 223table 1: a

summ

ary table of 15 published and three new records of X

erotyp

hlo

ps verm

icula

ris(M

er

re

M, 1820), along the B

ulgarian Black sea coast. L

ocalitynum

bers correspond to numbers in Fig. 1. n/a – no inform

ation available.

Locality

Locality nam

eL

atitude L

ongitude a

pproximate

altitude

Num

ber of H

abitatD

ate/tim

e source

number

(° N)

(° e)

accuracy [m]

(m a.s.l.)

individuals(if available)

1t

he „Maslen N

os“ Cape

42.3075727.79071

± 100 0-50

1n/a

1954-VB

esH

KO

V(1956)

2t

he „Maslen N

os“ Cape

42.3075727.79071

± 100 0-50

10in the soil

1955-VII-29

Be

sHK

OV

(1956) 3

the „M

aslen Nos“ C

ape42.30757

27.79071± 100

0-50 7

in the soil1955-V

III-2B

esH

KO

V(1956)

4t

he „Maslen N

os“ Cape

42.3075727.79071

± 1000-50

n/an/a

1957-VI-12

Be

sHK

OV

(1961) 5

the „M

aslen Nos“ C

ape42.30757

27.79071± 100

0-50 n/a

n/a1957-V

III-10B

esH

KO

V(1961)

6In the vicinity of K

iten, 42.22965

27.73703± 2,000

0-100 3

under stones 1970-V

IIIP

aPsD

Or

F(1971)

about 3 km from

the seasidein a gully

7a

brook valley between

42.0851027.94539

± 2,0000-50

1under stone

1970 Č

IHa

ř(1989)

ahtopol and V

eleka river

8 r

opotamo r

iver valley 42.31463

27.72854 ± 2,000

0-50 1

n/a 1970

ČIH

(1989) 9

arkutino

42.32887 27.72992

± 1,000 0-50

2 under a stone on a dry

1976 B

ar

tO

sIK(1981)

hill at the seaside10

arkutino

42.3288727.72992

± 1,0000-50

1roadkill

1977B

ar

tO

sIK(1981)

11N

ear arkutino

42.3274327.73388

± 1,500 0-50

2under a stone betw

een 1979-V

HN

eM

aN

N(1981)

dunes12

Dunes near a

rkutino42.32743

27.73388± 1,000

0-50 4

in a depression between

1980-VB

Use

Ke

(1982) dunes

13U

nfinished hotel complex

42.2873427.74953

±10 16

1 adultunder a stone

2009-VI-4/

this study

‟Perla 2” (1.5 km north

between abandoned

9:00(N

ikolay tz

aN

KO

V) of Prim

orsko)buildings

14a

bandoned hotel complex

42.3365927.72877

± 10 24

2 adults, under a stone

2010-III/t

his study ‟z

name N

a Mira” (0.5 km

1 juvenile

between abandoned

10:00-11:00(a

ndreist

OJa

NO

V) northeast of the

buildingsa

rkutino swam

p)15

about 0.5 km

north 42.338697

27.728478± 10

30 1 subadult

under a stone on 2017-V

I-5/t

his study of a

rkutinothe road in a bright

15:00(t

homas

re

ICH)

broadleaf forest16

‟sveti Ivan” Island 42.43832

27.69132± 500

0-50 n/a

n/an/a

BU

re

sCH

& z

ON

KO

Wnear sozopol

(1934)17

Mainland seaside vis-à-vis

42.3395927.72987

± 500 0-50

n/an/a

n/aB

esH

KO

V(1985)

‟zm

iyskia Ostrov” Island =

sveti toma

18C

oast north of arkutino

42.3439927.72416

± 1,000 0-50

n/ain a depression

n/at

HIe

Me

(1986)

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It is thus strongly suggested to con-serve sparsely forested sandy or rocky habi-tats, if necessary, by appropriate manage-ment, to provide suitable conditions for thespecies to survive in the studied region.

aCKNOWLeDGMeNts: this note is dedi-cated to two great friends and colleagues, † NikolaytzaNKOV and † andrei stOJaNOV, who passed away ina car accident on June 22, 2016. they had helped dur-ing the fieldwork and provided records. the work wassupported by the slovak research and Developmentagency under the contract No. aPVV-15-0147.

reFereNCes: aFsar, M. & ÇIÇeK, K. &taYHaN, Y. & tOK, C. V. (2016): New records ofeurasian Blind snake, Xerotyphlops vermicularis(MerreM, 1820) from the Black sea region of turkeyand its updated distribution.- Biharean Biologist,Oradea; 10: 93-97. BartOsIK, M. (1981): Gady okoli-cy rzeki ropotamo w Bulgarii.- Przeglad zoologiczny,Wrocław; 23 (3): 371-385. BesHKOV, V. (1956): theWorm snake in our country.- Priroda I znanie, sofija;4 (1956): 16-18. [In Bulgarian]. BesHKOV, V. (1961):Beitrag zur zoogeografischen Untersuchung derHerpetofauna in Bulgarien.- Izvestija na zoologi -českija Institut s Muzej / Bulletin de l’Institut dezoologie et Musée, sofia; 10: 373-383. [In Bulgarianwith German summary]. BesHKOV, V. (1985): am -phibia, reptilia; pp. 32-41. In: BOteV, B. & PesHeV, t.(eds.): red data book of the People’s republic ofBulgaria. Vol. 2. animals. sofija (Bulgarian academyof sciences - Bas). [In Bulgarian]. BesHKOV, V.(1998): Bulgaria’s amphibians and reptiles; pp. 395-409. In: MeINe, C. (ed.): Bulgaria’s biological diversi-ty: Conservation status and needs assessment; Vols. Iand II. sofija & Moskva (Pensoft). BesHKOV, V. &NaNeV, K. (2006): amphibians and reptiles inBulgaria. sofia & Moskva (Pensoft), pp. 120. BUresH,I. & zONKOW, J. (1934): Untersuchungen über dieVerbreitung der reptilien und amphibien in Bulgarienund auf der Balkanhalbinsel. II teil: schlangen (ser -pentes). Mitteilungen aus den Königlichen Natur -wissenschaftlichen Instituten in sofia, sofija; 7: 106-188. [In Bulgarian with German summary]. BUseKe,D. (1982): Die schlangen der südbulgarischenschwarzmeerküste.- sauria, Berlin; 4 (2): 5-9. ČIHař,J. (1989): Na jih od sofie. Praha (albatros), pp. 93-110.[In Czech]. FILIPOVa-MarINOVa, M. & GIOsaN, L. &aNGeLOVa, H. & PreIsINGer, a. & PaVLOV, D. &VerGIeV, s. (2011): Palaeoecology of submerged pre-historic settlements in sozopol Harbour, Bulgaria; pp.230-244. In: BeNJaMIN, J. & BONsaLL, C. & PICKarD,C. & FIsCHer a. (eds.): submerged prehistory; Oxford(Oxbow books). GrILLItsCH, B. & GrILLItsCH, H.(1993): Typhlops vermicularis MerreM, 1820 -Wurmschlange oder Blödauge; pp. 15-32. In: BöHMe,W. (ed.): Handbuch der reptilien und amphibieneuropas; vol. 3/1, schlangen (serpentes) I; Wiesbaden(aula). JaBLONsKI, D. & stLOUKaL, e. (2012):supplementary amphibian and reptilian records fromeuropean turkey.- Herpetozoa, Wien; 25: 59-65.JaBLONsKI, D. & BaLeJ, P. (2015): Xerotyphlops ver-micularis (MerreM, 1820), in the west Bulgarianrhodope Mountains: rediscovery after more than 100years.- Herpetozoa, Wien; 27: 200-203. KereY, I. e. &MerIÇ, e. & tUNOğLU, C. & KeLLING, G. & BreNNer,r. L. & DOğaN, a. U. (2004): Black sea–Marmara sea

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KeY WOrDs: reptilia: squamata: serpentes:typhlopidae; Xerotyphlops vermicularis, chorology,distribution, new records, colonization route, ecology,habitat, isolated population, Bulgaria

sUBMItteD: January, 31, 2018

aUtHOrs: Daniel JaBLONsKI (Correspondingauthor < [email protected] >) 1), Petr BaLeJ 2),thomas reICH 3) & Borislav NaUMOV 4)

1) Department of zoology, Comenius Universityin Bratislava, Ilkovičova 6, Mlynská dolina, 842 15Bratislava, slovakia.

2) zdeňka Bára 114/4, 70030 Ostrava, Czechrepublic.

3) CH-5611 anglikon, switzerland4) Institute of Biodiversity and ecosystem

research, Bulgarian academy of sciences, 2 YuriiGagarin street, 1113 sofia, Bulgaria.

224 sHOrt NOte HerPetOzOa 31 (3/4) Wien, 28. Februar 2019 sHOrt NOte

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