Hyla 2015 no1 by Dušan Jelić

Vol. 2015., No 1., July 2015.

herpetological bulletin

Croatian Herpetological Society HYLA

Hyla herpetološki bilten herpetological bulletin Vol. 2015., No 1.

Urednik/Editor: dr. sc. Dušan Jelić

Hrvatsko herpetološko društvo - HYLA Croatian Herpetological Society - HYLA

Zagreb, July 2015.

Impressum HYLA, HERPETOLOGICAL BULLETIN Ključni naslov: Hyla (Zagreb) Skraćeni ključni naslov: Hyla (Zagreb) Naslovna fotografija/Front page photo: Chameleo africanus (Maria DiMaki) Izdavač/Publisher: Hrvatsko herpetološko društvo - HYLA Croatian Herpetological Society - HYLA, Lipovac I., br. 7, HR-10000 Zagreb, Croatia Urednik/Editor: dr. sc. Dušan Jelić, jelic.dusan@gmail.com Urednički odbor/Editorial board: dr. sc. Dušan Jelić, Croatia Toni Koren, Croatia dr. sc. Biljana Janev Hutinec, Croatia dr. sc. Ljiljana Tomović, Serbia dr. sc. Tomislav Bogdanović, Croatia dr. sc. Duje Lisičić, Croatia dr. sc. Konrad Mebert, Switzerland David Bird, UK Ivona Burić, Croatia ISSN: 1848-2007 http://hrcak.srce.hr/hyla

Urednik izdanja/Issue editor: dr. sc. Biljana Janev Hutinec bjanev.hutinec@gmail.com

Hrvatsko herpetološko društvo - HYLA Croatian Herpetological Society - HYLA

Hyla VOL. 2015., No. 1 ISSN: 1848-2007

Sadržaj: Contents:

O HHD HYLA / About HHD HYLA ………………………………….……………….…… 1

ÇIÇEK, K., AYAZ, D.

̶ Does the red-eared slider (Trachemys scripta elegans) breed in

Turkey?................................................................................................................................. 4 KLEEWEIN, A. ̶ Interactions between Emys orbicularis and allochthonous turtles of the family Emydidae at basking places ……………………………………...……………… 11 TZANKOV, N., POPGEORGIEV, G., KORNILEV, Y., NATCHEV, N., STOYANOV, A., NAUMOV, B., IVANCHEV, I. ̶ First survey on the invasive Pond slider (Trachemys scripta) in Bulgaria: historic development and current situation ….................................................................... 18 KLEEWEIN, A. ̶ Investigating temperature tolerance in wild broods of Trachemys scripta elegans (Reptilia: Testudines: Emydidae) in Austria ........................................................ 28 DIMAKI, M., CHONDROPOULOS, B., LEGAKIS, A., VALAKOS, E., VERGETOPOULOS, M. ̶ New data on the distribution and population density of the African Chameleon, Chamaeleo africanus and the Common Chameleon, Chamaeleo chamaeleon in Greece ................... 36 ĐORĐEVIĆ, S., ANĐELKOVIĆ, M. ̶ Possible reproduction of the red-eared slider, Trachemys scripta elegans (Reptilia: Testudines: Emydidae), in Serbia, under natural conditions .... 44 SCHWEIGER, M. ̶ First record of breeding of the alien turtle species Trachemys scripta elegans in the wild on the island of Krk, Croatia? ............................................................ 50 JELIĆ, L., JELIĆ, D. ̶ Allochthonous species of Turtles in Croatia and Bosnia and Herzegovina ............................................................................................................................................ 53 STOYANOV, A. ̶ Registered high mortality of allochthon Red-eared Sliders (Trachemys scripta elegans) in an artificial pond in Sofia, Bulgaria ………………………………… 65 GRANO, M., CATTANEO, C.

̶ A survey on the presence of the invasive alien American

bullfrog, Lithobates catesbeianus (Shaw, 1802) (Amphibia Anura Ranidae) in Latium (Central Italy) with reference to a possible infection of Batrachochytrium dendrobatidis on Bufo bufo ……………………………………………………………………………........ 70

O HHD – HYLA Hrvatsko herpetološko društvo – Hyla osnovano je 1997. godine pod imenom "Društvo za zaštitu i proučavanje vodozemaca i gmazova Hrvatske-Hyla". Osnovano je od strane biologa i zaljubljenika u vodozemce i gmazove zbog potrebe zaštite ovih životinja koje su često i bezrazložno proganjane i ubijane. Također se pojavila potreba za zaštitom ekosustava i mnogih staništa na kojima obitavaju ove, ali i ostale skupine životinja. Društvo je 2004. preimenovano u današnji naziv te sa razvila unutrašnja infrastruktura u vidu web stranice (www.hyla.hr) i mailing liste koje održavaju povezanost članova i mreže regionalnih i lokalnih udruga i organizacija partnera. Društvo je registrirano kao strukovna organizacija te je većina članova biološke struke. Međutim, otvoreni smo za sve koje zanima zaštita i proučavanje hrvatske herpetofaune (vodozemaca i gmazova) i staništa. HHD-Hyla je punopravna članica IUCN (International Union for Conservation of Nature), najstarije i najveće međunarodne mreže za zaštitu prirode koja pod svojim okriljem okuplja više od 1000 članica - nevladinih i državnih organizacija - u više od 160 zemalja širom svijeta. HHD-Hyla je od 2012. članica udruženja udruga Hrvatski institut za biološku raznolikost HIB zajedno sa svojim partnerima Udrugom za biološka istraživanja – BIOM, Hrvatskim društvom za biološka istraživanja HDBI i Hrvatskim mirmekološkim društvom HMD. Projekti i aktivnosti usmjereni su na istraživanja te zaštitu vrsta i staništa, edukaciju lokalnog stanovništva i šire javnosti (u sklopu projekata ali i zasebna predavanja i radionice), edukaciju studenata te izdavanje publikacija i ostalog edukativnog materijala. Društvo je aktivno na nacionalnoj razini te provodimo projekte u raznim dijelovima Hrvatske uz suradnju s državnim i lokalnim institucijama, udrugama, stručnjacima u zemlji i inozemstvu, školama te lokalnim stanovništvom.

KONTAKT Poštanski pretinac: Lipovac I., br. 7, HR-10000 Zagreb Telefon: 01/2348279 (ured) e-mail: info@hhdhyla.hr http://www.hhdhyla.hr

About HHD - HYLA Croatian Herpetological Society - Hyla was founded in 1997 under the name "Society for the protection and study of amphibians and reptiles in Croatia-Hyla". It was established by the biologists and nature enthusiasts because of the need to protect amphibians and reptiles which are often unduly persecuted and killed. The need for protection of ecosystems and many habitats, on which this and other groups of animals reside, also occured. In 2004 Society was renamed to its present name and we developed an infrastructure, web site (www.hyla.hr) and mailing list, through which we maintain cohesion between members and a network of regional and local NGOs and partner organizations. Society is registered as a professional organization, and the majority of our members are biologists. However, we are open to all people interested in research and conservation of Croatian herpetofauna (amphibians and reptiles) and habitats. HHD-Hyla is a full member of the IUCN (International Union for Conservation of Nature), the oldest and largest international network for the protection of nature, with more than 1000 members - government and non-government organizations - in over 160 countries around the world. HHD-Hyla is since 2012 a full member and the founding party of the Croatian Instiute for Biodiversity CIB together with its partners Association for Biological Research â&#x20AC;&#x201C; BIOM, Croatian Biodiversity Research Society HDBI and Croatian Mirmecological Society HMD. Projects and activities are focused on research and protection of species and habitats, education of the local inhabitants and public (during the projects, as well as separate lectures and workshops), training of students and publishing of the various scientific, professional and educational materials. Society is active at the national level and implements projects in different parts of the Croatia in cooperation with national and local institutions, NGOs, national and international experts and scientists, schools and local inhabitants.

CONTACT Address: Lipovac I., no. 7, HR-10000 Zagreb Telephone: 01/2348279 (office) e-mail: info@hhdhyla.hr http://www.hhdhyla.hr

Hyla VOL. 2015., No. 1 ISSN: 1848-2007

Short Note Çiçek & Ayaz 2015

Hyla

VOL. 2015., No.1, Str. 4 - 10 ISSN: 1848-2007

Does the red-eared slider (Trachemys scripta elegans) breed in Turkey? Da li se crvenouha kornjača (Trachemys scripta elegans) razmnožava u Turskoj? KERIM ÇIÇEK1*, Dinçer AYAZ1 1

Section of Zoology, Department of Biology, Faculty of Science, Ege University, 35100, Izmir, Turkey. kerim.cicek@hotmail.com or kerim.cicek@ege.edu.tr

Abstract Here, we report for the first time reproduction in a naturalized population of the red-eared slider (Trachemys scripta elegans) from Southern Anatolia (Anamur, Mersin). We detected a female laying 15 eggs in the morning of July 03. 2012 and a female digging nest on May 16. 2015. Moreover, two hatchlings 26.1mm and 28.4mm in length were observed on September 03. 2013. According to our observations, the Mediterranean coast of Turkey has the potential to provide the requirements of the species. The described impacts of the red-eared sliders on native turtles are competition for food and basking sites.

Key words: alien species, naturalized population, Trachemys scripta elegans, Anatolia

Sažetak Po prvi puta izvještamo o reprudukciji u udomaćenoj populaciji crvenouhe kornjače (Trachemys scripta elegans) iz južne Anatolije (Anamur, Mersin). Opazili smo ženku koja je izlegla 15 jaja ujutro, 3. lipnja 2012., te ženku koja je kopala gnijezno 16. svibnja 2015. Dana 23. Rujna 2013 opazili smo i dva netom izvaljena mladunca, dužine 26.1 mm i 28.4 mm dužine. Sukladno našim opažanjima, Mediteranska obala Turske ima potencijal da ispunjava potrebe ove vrste. Utjecaj crvenouhe kornjače na nativne populacije kornjača je kompeticija za hranu i mjesta za sunčanje. Ključne riječi: strane vrste, udomaćena populacija, Trachemys scripta elegans, Anatolia

The global introduction of non-native

recognized as having three subspecies (T. s. scripta,

amphibians and reptiles has increased exponentially

T. s. troostii, and T. s. elegans, ERNST ET AL.,

through the past 150 years, these mostly originated

1994), The Red-eared Slider T.s.elegans is ranked

from North America, the numbers of turtle

among the world’s 100 most invasive species

introductions are greater than other taxa (Kraus

(LOWE ET AL., 2000). The species is the most

2009). One of the main factors in the expansion of

popular pet turtle worldwide since the 1950s due to

non-native species is commercial trade and about

its reasonably low price and simple husbandry

64 turtles and tortoise species have been widely

(Ficetola et al. 2012). The red-eared sliders

kept as pets by reptile enthusiasts (see Reptiles

(Trachemys scripta elegans) have been generated

Magazine, 2015). Trachemys scripta (Slider) is a

on farms in the USA for pet trade since the 1970s

medium-sized

and were the most widely traded species in Europe 4

semiaquatic

turtle,

currently

Short Note Çiçek & Ayaz 2015

Hyla

VOL. 2015., No.1, Str. 4 - 10 ISSN: 1848-2007

(Scalera 2006). However the EU banned its trade

[province of Mersin, Lat: 36.081789, 32.894666,

starting in 1997 (Regulation 338/1997; Regulation

sea level] on the Mediterranean coast of southern

349/2003) due to the high risk of biological

Turkey (Figure 1A, B). Along the front of the castle

invasion (Ficetola et al. 2012). In this context, the

walls is a moat 1.5 – 2m in depth, 3m in width,

trade of the other two subspecies (T. s. scripta, T. s.

500m2 in area, and

troostii and its hybrids) has rapidly increased after

vegetation, the red-eared sliders share the biotope

prohibition (Scalera 2006).

with about 20 European pond turtles (Emys

containing dense aquatic

The red-eared sliders have been released or

orbicularis) and 400 Western Caspian turtles

escaped into natural or semi-natural wetlands in

(Mauremys rivulata). The turtles are in an

many parts of the world (Scalera 2006) and its

overcrowded space with a ratio of 1-2 turtles/m2

naturalized populations are reported in at least in 73

and have limited food, basking and nesting sites.

countries or overseas territories in Europe, Africa,

The nesting site of the turtles is limited to the space

Asia, Central and North America, South America

next to the moat. However, it was observed that

and Oceania (Lever 2003; Scalera 2006; Pupins

some females build their nests in some areas inside

2007; Kraus 2009; Pendlebury, 2009; Kikillus et al.

the castle, 20 - 30 m away from the moat. The

2010, Ficetola et al. 2012; van Dijk et al. 2013).

sliders may move up to 1.6 km to find a suitable

However, populations in some introduced areas are

nesting place and the nests are jug-shaped and up to

unable to reproduce because of low temperatures or

12 cm deep (Ernst et al. 1994; Bringsøe, 2006)

limited precipitation (Bringsøe 2001; Ficetola et al.

Local people stated that the red-eared

2009). Few naturalized populations have been

sliders successfully breed in the moat; however we

reported in Spain, France, Italy, Germany, Austria,

could not observe hatchling individuals from

Slovenia, Japan and southeast Asia, Australia, New

fieldwork up to 2012. In our fieldwork on July 03.

Zealand, in the West Indies and in the introduced

2012, we observed an egg-laying female in the

range in the US (Pleguezuelos 2002; Lever 2003;

morning (Figure 1C, D). The female laid 15 eggs

Cadi et al. 2004; Scalera; 2006, Ramsay et al. 2007;

with an average size of 36.0mm in length (SD=

Kikillus et al. 2010).

1.53, range= 33.58 – 37.66), 23.7mm in width (SD=

In our field trips all around Turkey from

1.01, range= 22.70 – 25.54). We also detected a

2003 to 2015, we observed the red-eared sliders

female digging a nest on May 16, 2015. The eggs of

which had been released by their owners to natural

the red-eared sliders are ovoid in shape, 30.9-43.0

or semi-natural wetlands in many cities in Thrace

mm long, and 19.4-25.6 mm wide (Ernst et al.

(Kırklareli, Istanbul) and western Anatolia (Izmir,

1994). The nest is jug-shaped, 14cm in depth, 8cm

Muğla) and southern Anatolia (Antalya, Mersin and

wide at the mouth and 17cm wide at the base

Adana). In interviews with the local people, we

(Figure 1D). The female had straight carapace

could not obtain satisfactory data about proven

length of 204mm, plastron length of 216mm and

reproduction of the sliders.

weight of 1735g (Figure 1E).

In 2005, we detected a naturalized population consisting of 10 – 15 adult, semi-adult and juvenile individuals in Mamure Castle, Anamur 5

Hyla

VOL. 2015., No.1, Str. 4 - 10 ISSN: 1848-2007

Short Note Çiçek & Ayaz 2015

Figure 1. A: general view biotope of the red-eared sliders, B: native species of E. orbicularis and M. rivulata in the habitat, C: nesting female, D: nest, E: egg-laid female, and F: hatchling Slika 1. A: Generalni pogled na stanište crvenouhe kornjače, B. nativne vrste E. orbicularis i M. rivulata u staništu, C: ženka koja polaže jaja u gnijezdo, D: gnijezdo, E: ženka koja polaže jaja u gnijezdo i F: mladunac. 6

Short Note Çiçek & Ayaz 2015

Hyla

VOL. 2015., No.1, Str. 4 - 10 ISSN: 1848-2007

Females could lay up to six clutches every

September 2013 (Figure 1F). In the native range,

year, varying 2-30 eggs in a clutch , incubation

the red-eared sliders hatchlings have carapaces of

period is 59 - 112 days and is extended in low

25.4-41.8 mm (Moll 1994; Ernst et al. 1994).

temperatures (Ernst et al. 1994; Bringsøe 2006).

According to our interviews, hatchlings emerged at

We were not able to observe the hatchings;

end of August and mid-September and thus within

however, the employees of the castle photographed

the approximate incubation duration 60 – 75 days.

two hatchlings with 26.1mm and 28.4mm SCL in

Figure 2. Climatogram of province Mersin from southern Turkey. (Turkish State Meteorological Service, 2015) Slika 2. Klimatogram provincije Mersin iz južne Turske. (Turkish State Meteorological Service, 2015)

Anamur has a Mediterranean climate

temperatures of 22 - 27°C become males, whereas

which has long, hot and dry summers with cool,

females develop at warmer temperatures (Ernst et

rainy winters. Average monthly temperature is

al. 1994). Besides, when we look at the native

19.1oC and average precipitation was 48.8kg/m2

distribution of the sliders (Ficetola et al. 2012), it

between

seems that almost all of Turkey is in same latitude

1954

and

2015

(Turkish

state

meteorological service 2015, Figure 2). In the breeding and incubation period (May - September)

of their natural range. A

naturalized

population

20-30

of the Anamur population, average monthly air

individuals is present in the Izmir Wild Life Park in

temperature ranges between 21.3 – 28.3oC (Turkish

Western Anatolia. According to the interviews we

state meteorological service 2015). The sliders

conducted with the employees of the park and our

usually lay eggs from April to July in their native

own observations, it is presumed that the species

distribution, and development of eggs depends on

does not reproduce there. On the other hand, the

moisture and temperature (Tucker & Packard 1998;

Mediterranean coast of Turkey has the potential to

Ernst et al. 1994). The eggs that are incubated at

provide the requirements of the species. The 7

Short Note Çiçek & Ayaz 2015

Hyla

VOL. 2015., No.1, Str. 4 - 10 ISSN: 1848-2007

established breeding population we have identified

seems inevitable that the invasive turtle will

is an indicator of such potential.

generate pressure on many native species, notably

It has been reported that the red-eared

on European pond turtles, in the immediate future.

sliders are competing with European terrapins -

The Convention on Biological Diversity (CBD

European pond turtles (Emys orbicularis) and

2015) recommended a three-stage hierarchical

Spanish terrapins (Mauremys leprosa) for food,

approach

basking and nesting sites (Cadi & Joly 2003, 2004;

prevention,

Fıcetola et al. 2012). We also observed the

response,

competition of the sliders with the native terrapins

precautions to be taken on non-native species are:

of E. orbicularis and M. rivutala at Mamure castle.

the prohibition on the import of the sliders by

Especially E. orbicularis is repressed for food and

Turkish authorities, raising awareness in pet reptile

basking place by the other two turtle species. The

enthusiasts and, in addition, potential national

sliders are generally omnivores (Ernst et al. 1994)

sustainable management plans for controlling non-

and high density populations could even impact on

native species, designed by decision-makers in the

aquatic

near future.

vegetation,

macroinvertebrates

and

invasive

non-native

detection/surveillance control

and

species:

and

eradication.

rapid Primary

amphibian communities (Teıllac-deschamps & Prevot-julliard

2006).

The

species

also

Acknowledgements

considered a potential vector of Salmonella

We thank to Mamure Castle personnel Sami Vardar

(Nagano et al. 2006) and the epidemiological risk

and Recep Tüfenk for their kindly help and share

has led to a national ban of sales of sliders since

their observation with us. This study is financially

1975 in the US (Ernst et al. 1994; Scalera 2006).

supported

Besides, the red-eared sliders could cause the risk

103T189, 110T927 and 112T913] and EBILTEM

of transmission of pathogens to native terrapins

2007BIL012, [2013BIL013]. We are indebted to

(Hidalgo-vila et al. 2009).

these organizations for financial support.

TUBITAK

[Project

numbers:

Rödder et al. (2009) modeled a potential distribution of Trachemys scripta according to some essential physiological and reproductive characteristics, and observed there are vast suitable areas that could provide the requirements of the species in North, Central and South America, Europe, West and Central Africa, the East African coast, eastern Asia, and the eastern and western parts of Australia, and Turkey. Our observation also supported the model (Rödder et al. 2009) and demonstrated that southern Anatolia is quite suitable for the reproduction of the species. In Turkey, red-eared sliders are sold at pet shops for 23 euros and there is no monitoring. Therefore, it

References Bringsøe, H. (2001): Trachemys scripta (Schoepff, 1792) – Buchstaben-Schmuckschildkröte. pp. 525–583. In Fritz, U. (eds.). Handbuch der Reptilien und Amphibien Europas. Schildkröten (Testudines). AULA. Bringsøe, H. (2006): NOBANIS. Invasive Alien Species Fact Sheet Trachemys scripta, <http://www.nobanis.org/files/factsheets/Trachem ys_scripta.pdf>. Accessed: 27 February 2015. Cadi, A., Delmas, V., Prévot-Julliard, A. C., Joly, P., Pieau, C., Girondot, M. (2004): Successful reproduction of the introduced slider turtle (Trachemys scripta elegans) in the south of France. Aquatic Conservation: Marine and Freshwater Ecosystems 14(3): 237–246. Cadi, A., Joly, P. (2003): Competition for basking places between the endangered European pond turtle (Emys orbicularis galloitalica) and the introduced red-eared slider (Trachemys scripta 8

Hyla

VOL. 2015., No.1, Str. 4 - 10 ISSN: 1848-2007

elegans). Canadian Journal of Zoology 81: 1392– 1398. Cadi, A., Joly, P. (2004): Impact of the introduction of the red-eared slider (Trachemys scripta elegans) on survival rates of the European pond turtle (Emys orbicularis). Biodiversity and Conservation 13: 2511–2518. CBD (2015): Invasive Alien Species. Programmes and Issues. CBD - Convention on Biological Diversity, <http://www.cbd.int/programmes/crosscutting/alien/>. Accessed: 18 February 2015. Ernst, C. H., Lovich, J. E., Barbour, R. W. (1994): Turtles of the United States and Canada. Smithsonian Institution Press, Washington and London. Ficetola, G. F., Thuiller, W., Padoa-Schioppa, E. (2009): From introduction to the establishment of alien species: Bioclimatic differences between presence and reproduction localities in the slider turtle. Diversity and Distributions 15: 108–116. Ficetola, G.F., Rödder D., Padoa-Schioppa, E. (2012): Trachemys scripta (Slider terrapin). In: Handbook of global freshwater invasive species. pp. 331-339. In: Francis, R. (eds.) Earthscan, Taylor & Francis Group Abingdon, UK. GISD (2015): Trachemys scripta elegans. GISD Global Invasive Species Database. <http://www.issg.org/database/species/ecology.as p?si=71>. Accessed: 25 February 2015. Hidalgo-Vila, J., Díaz-Paniagua, C., Ribas, A., Florencio, M., Pérez-Santigosa, N., Casanova, J. C. (2009): Helminth communities of the exotic introduced turtle, Trachemys scripta elegans in Southwestern Spain: Transmission from native turtles. Research in Veterinary Science 83: 463– 465. Kikillus, K. H., Hare, K. H., Hartley, S. (2010): Minimizing false-negatives when predicting the potential distribution of an invasive species: A bioclimatic envelope for the red-eared slider at global and regional scales. Animal Conservation 13(suppl. 1): 5–15. Kraus, F. (2009): Alien Reptiles and Amphibians: a Scientific Compendium and Analysis (Invading Nature - Springer Series in Invasion Ecology), Springer-Verlag. Lever, C. (2003): Naturalized Amphibians and Reptiles of the World. Oxford University Press, New York. Lowe S., Browne, M., Boudjelas, S., De Poorter, M. (2000): 100 of the World’s Worst Invasive Alien Species A selection from the Global Invasive Species Database. Published by The Invasive Species Specialist Group (ISSG) a specialist group of the Species Survival Commission (SSC) of the World Conservation

Short Note Çiçek & Ayaz 2015

Union (IUCN), 12pp. First published as special lift-out in Aliens 12 December 2000. Updated and reprinted version: November 2004. Moll, D. (1994): The ecology of sea beach nesting in slider turtles (Trachemys scripta venusta) from Carribean Costa Rica. Chelonian Conservation Biology 1(2):107-116. Nagano, N., Oana, S., Nagano, Y., Arakawa, Y. (2006): A severe Salmonella enterica serotype paratyphi B infection in a child related to a pet turtle, Trachemys scripta elegans. Japanese Journal of Infectious Diseases 59(2): 132-134. Pleguezuelos, J. M. (2002): Las especies introducidas de anfibios y reptiles. pp. 501–532. In: Pleguezuelos, J.M., Márquez, R., Lizana, M. (eds.) Atlas y Libro Rojo de los anfibios y reptiles de España. Dirección General de Conservación de la Naturaleza-Asociación Herpetológica Española. Pupins, M. (2007): First report on recording of the invasive species Trachemys scripta elegans, a potential competitor of Emys orbicularis in Latvia. Acta Universitatis Latviensis – Biology 723: 37–46. Ramsay, N. F., Ng, P. K. A., O’Riordan, R. M., Chou, L. M. (2007): The red-eared slider (Trachemys scripta elegans) in Asia: a review. pp. 161–174. In: Gherardi, F. (eds.) Biological invaders in inland waters: profiles, distribution, and threats. Springer Publishing. Reptiles Magazine (2015): < http://www.reptilesmagazine.com/>. Accessed: 23 February 2015. Rödder, D., Schmidtlein, S., Veith, M., Lötters, S. (2009): Alien invasive slider turtle in unpredicted habitat: A matter of niche shift or of predictors studied? PLoSONE 4: 7843. Scalera, R. (2006): Trachemys scripta. From: DAISIE (Delivering Alien Invasive Species Inventories for Europe).< www.europealiens.org>. Accessed: 23 February 2015. Teillac-Deschamps, P., Prevot-Julliard, A. C. (2006): Impact of exotic slider turtles on freshwater communities: an experimental approach. pp. 162–163. In: First European congress of conservation biology. Society for Conservation Biology, Heger, Hungary. Tucker, J. K., Packard, G. C. (1998): Overwinter survival by hatchling sliders (Trachemys scripta) in West-Central Illinois’. Journal of Herpetology 32: 431–434. Turkish State Meteorological Service (2015): <http://www.mgm.gov.tr/veridegerlendirme/il-veilceler-istatistik.aspx?m=MERSIN>. Accessed: 23 February 2015. van Dijk, P. P., Harding, J., Hammerson, G. A. (2013): Trachemys scripta. The IUCN Red List of 9

Hyla

VOL. 2015., No.1, Str. 4 - 10 ISSN: 1848-2007

Short Note ร iรงek & Ayaz 2015

Threatened Species. Version 2014.1. <www.iucnredlist.org>. Accessed: 23 February 2015.

Original Scientific Paper Kleewein 2015

Hyla

VOL. 2015., No.1, Str. 11- 17 ISSN: 1848-2007

Interactions between Emys orbicularis and allochthonous turtles of the family Emydidae at basking places Interakcije između Emys orbicularis i alohtonih kornjača porodice Emydidae na mjestima za sunčanje ANDREAS KLEEWEIN

University of Vienna, Department of Integrative Zoology, Althanstraße 14, A-1090 Vienna, Austria e-mail: andreas.kleewein@gmx.net

Abstract There are frequent remarks in literature of the supposed negative effects of Trachemys scripta elegans on Emys orbicularis. These competition effects pertain, in particular, to the securing of ideal basking places. A study under near-natural conditions now paints a different picture. Seven Emys orbicularis individuals were placed in an enclosure with 67 allochthonous turtles of 12 different species belonging to the family Emydidae. All interactions regarding basking places were recorded. Of a total of 149 interactions, 105 (70.5%) were neutral and therefore without consequence. Of the 44 negative interactions (29.5%), 19 had a negative result for E. orbicularis while 25 were negative for the allochthonous species. The study therefore indicates that there are no negative consequences of allochthonous species on E. orbicularis regarding behavior at basking places. A comparison of basking place selection revealed that allochthonous species are opportunistic compared to E. orbicularis. In a total of 124 observed cases, E. orbicularis selected half-shaded wood most frequently, followed by fully sun exposed wood and fully sun exposed rocks. During 42 recordings, basking duration of E. orbicularis at a given place ranged from 2 to 200 minutes, averaging 37 minutes.

Key words: Emydidae, interactions, basking place, basking place preference

Sažetak Postoje brojni literaturni navodi o navodnom štetnom djelovanju Trachemys scripta elegans na Emys orbicularis. Kompeticija između ove dvije vrste, barem djelomično, zavisi o osiguravanju idealnog mjesta za sunčanje. Ova studija, provedena u poluprirodnim uvijetima, prikazuje dosta drugačije rezultate. Sedam jedinki vrste Emys orbicularis stavljene su zatvoreni prostor sa 67 jedinki alohtonih kornjača svrstanih u 12 različitih vrsta iz porodice Emydidae. Tijekom eksperimenta bilježene su sve interakcije vezane uz odabir mjesta za sunčanje. Od ukupno 149 interakcija, 105 (70,5 %) ih je bilo neutralno i time bez posljedica. Od 44 negativne interakcije (29,5 %), 19 ih je imalo negativne posljedice za E. orbicularis dok ih je 25 imalo negativne posljedice za jedinku alohtone vrste. Studija pokazuje da alohtone vrste nemaju značajan negativan utjecaj na E. orbicularis u aspektu ponašanja pri odabiru mjesta za sunčanje. Usporedba odabira mjesta za sunčanje otkriva da su alohtone vrste oportunisti u usporedbi sa E. orbicularis. U totalno 124 zabilježena promatranja, jedinke vrste E. 11

Original Scientific Paper Kleewein 2015

Hyla

VOL. 2015., No.1, Str. 11- 17 ISSN: 1848-2007

orbicularis su odabrale polu zasjenjenu drvenu podlogu za sunčanje, dok ih je značajno manje odabralo potpuno osunčano drvo ili potpuno osunčani kamen. U 42 opažanja, jedinke vrste E. orbicularis zadržale su se na odabranom sunčalištu od dvije do 200 min, uz prosijek od 37 min. Ključne riječi: Emydidae, interakcije, mjesta za sunčanje, preference mjesta za sunčanje

species

INTRODUCTION

belonging

the

family

Emydidae:

In Europe, proven or potential negative

Trachemys scripta elegans, Trachemys scripta

consequences of allochthonous turtle species of the

scripta, Trachemys scripta troostii, Pseudemys

family Emydidae,

peninsularis,

particularly of

the

genus

Pseudemys

nelsoni,

Pseudemys

Trachemys, provide regular material for discussion.

concinna concinna, Pseudemys concinna floridana,

Cadi & Joly (2003, 2004) pointed out negative

Chrysemys

effects for Emys orbicularis, regarding basking

pseudogeographica

places, if Trachemys scripta elegans also occurred

Graptemys

in the same pond. The opposite, however, was

Graptemys pseudogeographica khonii, as well as

found by Macchi et al. (2008). Basking is very

hybrids between Trachemys scripta elegans and

important for turtles and constitutes a considerable

Trachemys scripta scripta. All of these species are

portion of their daily routine. Basking increases

combined in the term “allochthonous species” for

body temperature, quickens the metabolism and

data evaluation. Seven E. orbicularis were placed

thereby also stimulates feeding (Jackson 1971;

in the same enclosure with the allochthonous

Kepenis & McManus 1974; Parmenter 1980). To

species, resulting in a proportion of E. orbicularis

date, there has been no study under near-natural

to allochthonous species of 1:9.

conditions

involving

greater

diversity

All

picta

bellii,

Graptemys

pseudogeographica,

pseudogeographica

direct

interactions

ouachitensis,

between

allochthonous species of the family Emydidae. The

orbicularis

aim of this study, therefore, was to replicate an

registered. “Interaction” was defined as any

extreme

carapace or extremity contact during positioning at

allochthonous turtles than E. orbicularis, and to

the basking places. Neutral interactions were

conduct the observations under near-natural habitat

without consequence for either individual. Negative

conditions.

interactions

scenario,

with

considerably

and

allochthonous

included

species

displacement

were

one

individual by another, pushing other individuals off MATERIAL AND METHODS The study was conducted from the end of

their basking places into the water, bite attacks and lying on another individual’s carapace.

June until the beginning of October 2011, in

Furthermore, the preferred basking places

roughly weekly intervals (a total of 21 field days of

of E. orbicularis regarding material and sun

about five hours per day, in the open-air turtle

exposure were evaluated. The study enclosure

enclosure of the Reptile Zoo Happ (WGS84

provided rocks, tree-trunks, branches and reeds as

14°15‘56‘‘/46°37‘10‘‘; 441 m a.s.l.). The enclosure

basking places. Intensity of sun exposure was

offers near-natural conditions with an abundance of

classed as shaded, half-shaded and full sun

structures that can be used as basking places. The

exposure. Basking duration of E. orbicularis at a

enclosure contains 67 turtles of the following

given basking place was also measured. 12

Original Scientific Paper Kleewein 2015

Hyla

VOL. 2015., No.1, Str. 11- 17 ISSN: 1848-2007

A bite attack was observed in a single case only,

RESULTS Over the entire observation period, a total

when

male

orbicularis

bit

allochthonous species.

of 149 interactions were noted. The majority of

Three cases of intraspecific competition

these (n=105) were brief carapace or extremity

were observed in E. orbicularis, including a bite

contacts, which occurred on the way to a basking

attack, displacement from the basking place and

place and were without consequence for either

being pushed into the water.

individual (see Fig. 1). This was usually observed

During the course of the study, it became

when a turtle emerged from the water or was

apparent that allochthonous species differ from E.

searching for a suitable basking place on land. Once

orbicularis in that they do not seem to differentiate

the moving individual had found its optimal

between wood and rock basking places. For this

basking place, there was no further interaction.

reason, the allochthonous species’ preferences

These neutral interactions made up 70.5% of the

regarding basking place were not quantified. A total

total observed interactions.

of 124 observations of basking place preference

Negative interactions were observed much

were made for E. orbicularis during the course of

less frequently. A total of 44 (29.5%) negative

the study. Wood structures were selected most often

interactions were observed, including covering

(n=90). Rocks (n=27) and reeds (n=7) were rarely

another individual’s carapace, pushing another

used as basking places. Half-shaded (n=56) and full

individual from its basking place into the water,

sun exposure (n=55) basking places were selected

displacing another individual and bite attacks. Of

roughly equally, while shaded basking places

these 44 negative interactions, 43.2% (n=19)

(n=13) – as expected – were very rarely used.

affected E. orbicularis, while 56.8% (n=25)

Results

therefore

show

marked

affected allochthonous species. This indicates a

preference of E. orbicularis for half-shaded wood

slight

basking places (n=46) over fully sun exposed wood

advantage

orbicularis

over

allochthonous species. Only twice was a basking E. orbicularis

(n=31), fully sun exposed rock (n=19) and shaded wood

basking

places

(n=11).

All

further

pushed aside a few centimetres by an allochthonous

combinations were only observed very rarely (see

species. The opposite was observed three times.

Fig. 2). E. orbicularis also switched from one

Allochthonous species could be observed lying on the carapace of E. orbicularis six times,

basking place to another more frequently than could be observed for the allochthonous species.

however the opposite was the case 15 times. On the

Basking duration at a given place was

other hand, E. orbicularis individuals were pushed

measured 42 times for E. orbicularis, ranging from

from their basking places into the water 11 times,

2 to 200 min. The overall average basking duration

while this happened to allochthonous species only

at a given place was 37 min. In 12% of the cases

six times.

(n=5 time measurements), basking lasted between

Even once the water level had risen after

130 and 200 min at one place, always in the half-

extended rainfall and basking places became scarce,

shade.

no marked increase in aggressive behaviour or

measurements), basking duration at one place lasted

negative competition for basking places could be

between 2 and 63 min, at an average of 20 min.

88%

the

cases

(n=37

time

observed. 13

Original Scientific Paper Kleewein 2015

Hyla

VOL. 2015., No.1, Str. 11- 17 ISSN: 1848-2007

120

105

n interactions

100 80 60 40 20

type of interaction Figure 1. Interactions between E. orbicularis (Eo) and allochthonous species (A) at basking places. White = neutral/without consequence; grey = negative for allochthonous species; black = negative for E. orbicularis. Slika 1. Interakcije između E. orbicularis (=Eo) I alohtonih vrsta (A) na mjestima za sunčanje. Bijela boja =

n observations at basking places

neutralna/bez posljedica; siva = negativna za alohtone vrste; crna = negativna za E. orbicularis.

50 45 40 35 30 25 20 15 10 5 0

material/sun exposure Figure 2. Comparison of basking place preference of E. orbicularis regarding material and sun exposure. Slika 2. Usporedba sklonosti ka mjestima za sunčanje kod vrste E. orbicularis u odnosu na material i ekspoziciju. 14

Original Scientific Paper Kleewein 2015

Hyla

VOL. 2015., No.1, Str. 11- 17 ISSN: 1848-2007

on top of the carapace of T. s. elegans because it

DISCUSSION The study revealed that there are no negative

consequences

through

interspecific

was influenced negatively by T. s. elegans, thereby suffering a thermoregulatory disadvantage.

competition regarding basking places under near-

Bite attacks are certainly an exceptional

natural conditions. Under strictly experimental

form of interaction, but they were observed during

conditions, however, such negative consequences

this study and have also been observed in the

were confirmed by Cadi & Joly (2003, 2004), for

Donau-Auen National Park. In all cases, the attacks

example.

emanated from E. orbicularis males and targeted T.

During basking, the lightâ&#x20AC;&#x2122;s angle of

s. elegans females. Thus, they could be a form of

incidence and intensity, as well as air temperature

aggressive courtship behaviour.

and movement are crucial factors (Boyer 1965).

Turtles position themselves so that a maximum of

competition with the same negative interactions

their body surface faces the sun. Displacement from

was observed in E. orbicularis.

a chosen basking place affects thermoregulation

Similar preferences of T. s. elegans and E.

through a change to the lightâ&#x20AC;&#x2122;s angle of incidence.

orbicularis regarding basking place, such as

In basking piles, meanwhile, the top animal casts a

described by Cadi & Joly (2003), could not be

shadow on the lower animals which are, thus, at a

determined in this study. The allochthonous species

disadvantage.

body

were much more opportunistic in their choice of

dimensions of the allochthonous species such as

basking place, while E. orbicularis showed a clear

Trachemys scripta (SCL max 30 cm) and

preference for half-shaded wood and fully sun

Graptemys pseudogeographica (SCL max 27 cm)

exposed wood.

Thanks

the

greater

must

not

forgotten

that

intraspecific

(Ernst & Lovich 2009) compared to E. orbicularis

It was conspicuous that E. orbicularis

(SCL max 23 cm) (Fritz 2003), one would expect

mostly only stayed at a given basking place for very

E. orbicularis to be at a disadvantage in basking

short intervals. This is related to its smaller body

place competition (figure 3). This indeed appeared

size and due to faster warming and overheating.

to be true in the 11 cases where an E. orbicularis

Overall, it appears that E. orbicularis is indeed able

individual was pushed into the water by an

to assert itself against larger allochthonous species.

allochthonous species (versus only six opposite

Even after three years in the same pond, no

cases). The opposite, however, was observed in the

mortality of E. orbicularis occurred in the open-air

15 cases (versus only six opposite cases) where E.

enclosure of the Reptile Zoo Happ, although it had

orbicularis, due to its smaller size, was more able

been observed by Cadi & Joly (2004) in their

to climb on top of the carapaces of adult

experimental set-up. Nevertheless, the trade in

allochthonous species, thus gaining an advantage

animals ought to be more strictly regulated, and

(figure 4). In other turtle species, on the other hand,

allochthonous turtles ought to be removed from the

the mere presence of another species can have a

wild in the interest of animal, species and

negative effect. Polo-Cavia et al. (2010) showed

environmental protection.

that Mauremys leprosa, for example, would not pile

Hyla

VOL. 2015., No.1, Str. 11- 17 ISSN: 1848-2007

Original Scientific Paper Kleewein 2015

Figure 3. Adult E. orbicularis have smaller body sizes than allochthonous species (photo: A. Kleewein) Slika 3. Odrasli E. orbicularis imaju manju veličinu rijela nego alohtone vrste (fotografija: A. Kleewein)

Figure 4. E. orbicularis was found on the carapace of allochthonous species more frequently than vice versa. (photo: A. Kleewein) Slika 4. E. orbicularis pronađen na karapaksu alohtionih vrsta češće nego obrnuto (fotografija: A. Kleewein)

Original Scientific Paper Kleewein 2015

Hyla

VOL. 2015., No.1, Str. 11- 17 ISSN: 1848-2007

REFERENCES

ACKNOWLEDGEMENTS

Boyer, D.R. (1965): Ecology of the basking habit in turtles. Ecology 46: 99-118. Cadi, A. & Joly, P. (2003): Competition for basking places between the endangered European pond turtle (Emys orbicularis galloitalica) and the introduced red-eared slider (Trachemys scripta elegans). Canadian Journal of Zoology 81: 13921398. Cadi, A. & Joly, P. (2004): Impact of the introduction of the red-eared slider (Trachemys scripta elegans) on survival rates of the European pond turtle (Emys orbicularis). Biodiversity and Conservation 13: 2511-2518. Ernst, C.H. & Lovich, J.E. (2009): Turtles of the United States and Canada. Second Edition. John Hopkins University Press, Baltimore. Fritz, U. (2003): Die Europäische Sumpfschildkröte (Emys orbicularis). Supplement der Zeitschrift für Feldherpetologie 1, Laurenti-Verlag Bielefeld, 224 S. Jackson, D.C. (1971): The effect of temperature on ventilation in the turtle, Pseudemys scripta elegans. Respir. Physiol. 12: 131–140. Kepenis, V. & McManus, J.J. (1974): Bioenergetics of young painted turtles Chrysemys picta. Comp. Biochem. Physiol. A, 48: 309-317. Macchi, S., Balzarini, L. L. M., Scali, S., Martinoli, A. & Tosi, G. (2008): Spatial competition for basking sites between the exotic slider Trachemys scripta and the European Pond Turtle Emys orbicularis. In: CORTI C. (Ed.): Herpetologia Sardiniae. Edizioni Belvedere, Latina: 338-340. Parmenter, R.R. (1980): Effects of food availability and water temperature on the feeding ecology of pond sliders (Chrysemys scripta scripta). Copeia, 1998: 235–238. Polo-Cavia, N., Lopez, P. & Martin, J. (2010): Competitive interactions during basking between native and invasive freshwater turtle species. Biological Invasions 12 (7): 2141-2152.

Sincere thanks are due to the Reptile Zoo Happ in Klagenfurt, particularly to the directress Helga Happ,

for

allowing

the

observations

and

investigations for this study to take place. Thanks are also due to the Department for Integrative Zoology, especially to Walter Hödl, for material and professional support.

Original Scientific Paper Tzankov et al. 2015

Hyla VOL. 2015., No.1, Str. 18- 27 ISSN: 1848-2007

First survey on the invasive Pond slider (Trachemys scripta) in Bulgaria: historic development and current situation Prvo istraživanje invazivne crvenouhe kornjače (Trachemys scripta) u Bugarskoj: povijesni razvoj i trenutno stanje NIKOLAY TZANKOV1, GEORGI POPGEORGIEV2, YURII KORNILEV1, NIKOLAY NATCHEV4,5, ANDREY STOYANOV1, BORISLAV NAUMOV3, IVO IVANCHEV6 1

National Museum of Natural History, Bulgarian Academy of Sciences, 1 Tsar Osvoboditel Blvd., 1000 Sofia, Bulgaria, ntzankov@gmail.com 2 Bulgarian Society for the Protection of Birds, PO Box 50, 1111 Sofia, Bulgaria 3 Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, 2 Gagarin Str., 1113 Sofia, Bulgaria 4 Department of Integrative Zoology, Vienna University, Althanstrasse 14, 1090 Vienna, Austria 5 Faculty of Natural Science, Shumen University, Universitetska 115, 9700 Shumen, Bulgaria 6 Gea Chelonia Foundation, 10, Shipka str. 8239 Banya, Nessebar municipal, Bourgas district, Bulgaria Abstract Pond sliders (Trachemys scripta) have become a popular pet in Bulgaria since 1990. Through the years a number of released specimens were observed in the wild. Although the negative effects on native turtles have been studied extensively elsewhere, no specific studies (besides brief reports) have addressed the invasion of T. scripta in Bulgaria. The present study is based on over 25 years of field monitoring and represents the first source of detailed information on the distribution of the Pond slider in Bulgaria. A total of 293 UTM (10×10 km) squares with habitats suitable for freshwater turtles were surveyed. We collected 64 records for 173 individuals, from 19 UTM squares. From all observed individuals, only two were from the nominate subspecies – the rest belong to T. s. elegans. In our study only one subadult was observed. To date no successful hatching has been recorded, although successful overwinterings have been registered. We discuss various mitigation measures that must be rapidly initiated to limit future release of Pond sliders and to remove the non-native specimens from the Bulgarian ecosystems. Actions are demanded especially to avoid the potential epizootic events caused by parasites with highly lethal effect on native species. Such outbreaks might potentially have greater impact on the native pond turtle species than various forms of competition with T. scripta.

Key words: Bulgaria, Red-eared slider, pet trade, freshwater turtle communities, invasion, monitoring

Sažetak Crvenouha kornjača (Trachemys scripta) postala je popularni ljubimac u Bugarskoj od 1990. Kroz godine sve veći broj jedinki zabilježen je i u divljini. Iako su negativni učinci na izvornim kornjače su opsežno studirao negdje 18

Original Scientific Paper Tzankov et al. 2015

Hyla VOL. 2015., No.1, Str. 18- 27 ISSN: 1848-2007

drugdje, nema posebne studije (osim kratkih izvješća) obratili invaziju T. scripta u Bugarskoj. Ova studija se temelji na više od 25 godina praćenja na terenu i predstavlja prvi izvor detaljne informacije o raspodjeli Pond klizača u Bugarskoj. Ukupno 293 UTM (10 × 10 km) kvadrata sa staništa pogodna za slatkovodne kornjače ispitano. Prikupili smo 64 zapisa za 173 osoba, od 19 UTM kvadrata. Od svih promatranih osoba, samo dvije su od nominirati podvrste - ostatak pripada T. Š. elegans. U našem istraživanju je uočeno samo jednoga djeteta. Do danas nije uspješno leženja zabilježena, iako su registrirani uspješni overwinterings. Mi smo razgovarali o raznim mjere ublažavanja koje se moraju brzo pokrenut ograničiti buduće izdanje Ribnjak klizača i za uklanjanje ne-izvornih uzoraka s bugarskim ekosustava. Akcije su zahtijevali posebno da se izbjegne potencijalne epidemiološko događaja uzrokovanih parazitima s vrlo smrtonosnim učinkom na autohtonim vrstama. Takve pojave potencijalno mogu imati veći utjecaj na autohtone vrste kornjača jezerce od raznih oblika natjecanja s T. scripta. Ključne riječi: Bugarska, crvenouha kornjača, trgovina kućnim ljubimcima, slatkovodne kornjače, invazija, monitoring

Introduction In Europe, the local turtle communities

(e.g. Avery and Servan 1998, Bringsøe 2001, Cadi and Joly 1999, 2004).

consist of one or maximum two of the total four

The species has been reported to reproduce

freshwater species. On the Balkans these are the

successfully in various European countries, mostly in

European pond turtle Emys orbicularis (Linnaeus,

the southwestern part of the continent – Italy (Ferri

1758) and the Balkan pond turtle Mauremys rivulata

and Soccini 2003, Ficetola et al. 2003, Sperone et al.

(Valenciennes, 1833). The upper Pliocene period was

2010), Spain (Martinez-Silvestre 1997, De Roa and

relatively rich in large freshwater turtle communities

Roig 1997, Bertolero and Canicio 2000, Capalleras

that existed in Europe (cf. Młynarski 1976).

and Carretero 2000, Pleguezuelos 2004), and France

Thereafter, because of processes that were related to

(Cadi et al. 2004, Girondot et al. 2012). Sporadic

climate oscillations in the Pleistocene period, the

observations are published for other Europe countries:

species richness dropped significantly to the present

Austria (Gemel et al. 2005, Gutleb and Happ 2002,

levels.

Kleewein

2014),

Switzerland

(Wütrich

2004),

However, since the 1980s, due to their high

Slovenia (Vamberger et al. 2012). The reproductive

popularity in the pet trade, Pond sliders have been

performance of T. scripta in Southwestern Europe

exported all over the world, and are currently

was stated to show similar or even higher values than

distributed in the wild and in urban areas in nearly all

in native areas (Perez-Santigosa et al. 2008).

European countries (review in Bringsøe 2006).

In Bulgaria, Pond sliders were sold in high

Negative effects of released Pond sliders Trachemys

numbers (though specific quantities are unknown)

scripta (Thunberg in Schoepff, 1792) on European

since the 1990s and subsequently many specimens

freshwater ecosystems and especially on native

have been released in the wild by their owners.

freshwater turtles have previously been documented

However, published data on the species distribution 19

Original Scientific Paper Tzankov et al. 2015

Hyla VOL. 2015., No.1, Str. 18- 27 ISSN: 1848-2007

and its ecological impact in Bulgaria are generally

representing

missing. A brief review (with limited specific

freshwater turtles.

potentially

suitable

habitats

for

localities) was published in Stojanov et al. (2011),

When possible, exact geographic coordinates

where faunistic data were summarized and the authors

of each identified Pond slider were marked in situ

made the assessment that the Pond slider has

using handheld GPS units (accuracy ±5 m; Garmin,

established itself in the wild. Locally, the species was

Olathe, Kansas, USA). In few cases, locations were

mentioned for Vitosha Mountain (Tzankov et al.

identified via publicly available, high-resolution

2014). Thus, the present study is the first attempt to

geographically referenced satellite imagery from

summarize and present the current distribution and

2001–2014 (Google Earth 7; Google, Mountain View,

status of this invasive freshwater turtle.

California, USA). The dataset of slider presence/absence (but otherwise

Material and methods The dataset of Pond slider occurrence was

presence of native species) were summarized and plotted on the national 10×10 km UTM grid.

compiled from all available authors’ observations after 1990, with additional localities provided by

Results

colleagues. The data was collected during specific

Pond sliders were regularly encountered in

surveys for native freshwater turtles (E. orbicularis

Bulgaria from 1996. A total of 293 10×10 km UTM

and M. rivulata) and other freshwater herpetofauna,

squares with habitats suitable for freshwater turtles

as well as during incidental observations. Surveys

were surveyed. We collected a total of 64 records for

were performed throughout the country on various

173 individuals, from 19 UTM squares (6.4% of

natural, semi-natural, and urbanized bodies of water,

sampled UTMs; Fig. 1).

Original Scientific Paper Tzankov et al. 2015

Hyla VOL. 2015., No.1, Str. 18- 27 ISSN: 1848-2007

Figure 1. Distribution and relative abundance of observations of Trachemys scripta in Bulgaria (1990–2015) on a 10×10 km UTM grid. Slika 1. Distribucija I relativna abundance opažanja Trachemys scripta u Bugarskoj (1990-2015) na 10x10 km UTM mreži.

Nearly all observed specimens were adults

With distribution from the sea level up to

(or at least full-grown) except one sub-adult observed

1200 m a.s.l. (Dendrarium locality, Vitosha Mt.,

in an artificial pond in South Park in Sofia city. No

FN82; typographically misrepresented as 1300 m

male specimens were encountered in the field. In

a.s.l. in Stojanov et al. 2011), the identified area of T.

most of the localities, the sliders were presented by a

scripta completely overlaps that of the native pond

single specimen (63% of the localities).

turtles.

In all of the presented locations, the

Localities were mostly concentrated in urban

subspecies T. scripta elegans (Wied, 1838) was

or peri-urban zones of the big cites, i.e. Sofia (FN82,

observed, except in one case where two individuals of

FN92), Plovdiv (LG16), Burgas (NH30), Yambol

T. scripta scripta were observed once in the

(MH50), Ruse (MJ15), Pleven (LJ00) and Vidin

Stomopolou lagoon near the town of Primorsko

(FP46), where turtles were encountered in artificial

(UTM NG68).

ponds, canals, and slow flowing rivers (Table 1). Sliders have also been found in natural habitats 21

Original Scientific Paper Tzankov et al. 2015

Hyla VOL. 2015., No.1, Str. 18- 27 ISSN: 1848-2007

outside

settlements,

e.g.

at Managed

Reserve

Ropotamo (NG68) and Veleka (NG85). In certain

“Veliyov Vir” (NG58) and in natural habitats,

“hot-spots”, Pond sliders were observed multiple

commonly visited by people such as the mouths and

times over the years.

lower sections of the rivers Kamchiya (NH76),

Table 1. Localities and habitats of the observed adult Trachemys scripta elegans in Bulgaria (1996-2014). Tablica 1. Lokacije i staništa opaženih odraslih jedinki Trachemys scripta elegans u Bugarskoj (1996-2014). UTM

Easting

Northing

Locality

Habitat

Count

Date

FL89

23.263

41.459

Rupite

channel

1–12

1996–2014

FL89

23.263

41.461

Rupite

channel

2008

FL89

23.264

41.459

Rupite

channel

2014

FN82

23.228

42.628

Dendrariuma Vitosha Mtn

artificial pond

2006–2008

FN82

23.307

42.668

South Park 1, Sofia

artificial pond

1–12^

1997–2014

FN82

23.308

42.659

South Park 2, Sofia

artificial pond

1–5

1996–2009

FN92

23.342

42.685

Boris' Garden, Sofia

artificial pond

1–3

2005–2012

FN92

23.400

42.663

district Druzhba, Sofia

artificial pond

3–8

2006–2009

FN92

23.420

42.689

Sofia, eastern suburbs

artificial pond

2014

FN93

23.399

42.768

Negovan

artificial pond

2012–2013

FP46

22.858

43.946

Vidin

river

2011

GN03

23.469

42.705

Dolni Bogrov

artificial pond

late 1990s

LG16

24.746

42.154

Plovdiv, Maritsa River

river

2012

LG16

24.750

42.155

Plovdiv, Maritsa River

river

2004

MH50

26.492

42.487

Yambol

river

2002

MH99

26.965

43.288

near Shumen

artificial pond

2014

MJ15

25.941

43.837

Ruse

river

2004

NG39

27.423

42.450

Mandra Dam

terrestrial habitat

2014

NG58

27.710

42.300

Man. Reserve “Velyov Vir”

natural lake

2005

NG58

27.726

42.330

Ropotamo River

river

2012

NG58

27.728

42.303

Ropotamo River

river

2012–2013

NG68

27.730

42.315

Ropotamo River

river

2005

NG68

27.752

42.285

Lake Stomopolou

natural lake

2014

NG85

27.969

42.065

Veleka River

river

2005–2012

NH30

27.444

42.507

Burgas Lake

natural lake

2014

NH30

27.469

42.519

Atanasovsko Lake

channel (freshwater )

2013

NH55

27.673

42.948

Krivini

river

2013 22

Original Scientific Paper Tzankov et al. 2015

Hyla VOL. 2015., No.1, Str. 18- 27 ISSN: 1848-2007

NH76

27.886

43.022

Kamchiya River

river

2008

NH78

27.873

43.195

Varna Lake

natural pond

2000

^ – denotes one subadult individual; * – only observation of two individuals of T. s. scripta

Veleka River and Rupite are amongst the non-urban

successfully

localities with frequent observations of the Pond

concentration of individuals increased to several

slider.

hundred and even began to have an impact on the

for

many

years.

2010

the

The downstream of the Veleka River (UTM

waterfowl. In 2010/2011, the pond froze permanently

square NG85) was the subject of regular monitoring

for a prolonged period forming a thick layer of ice

of the population of the native freshwater turtles (E.

that likely led to depletion of oxygen in the water or

orbicularis,

Both

complete freezing of the water column. After the

autochthonous taxa inhabit syntopically this section.

thaw, seemingly the whole population in the pond

Sliders were observed only in the lowermost part

was observed dead. Stoyanov (2015) reports a similar

close to the river mouth. This section is with the

die-off in an artificial pond in 2005.

rivulata)

since

2005.

highest human presence and most probably the sliders

Notably, no breeding was detected in

are released there. The lower section of the river is

Bulgaria to date. It must be pointed out that in semi-

characterised by rapid water level fluctuations of ±2

natural conditions (such as in Sofia Zoo) sliders have

meters and changes in salinity (from freshwater to

been repeatedly observed to lay eggs, but no

brackish) due to buildup/breakage of a sandbar at the

successful

mouth. In these extreme conditions, the released

documented, although the reasons for the failure are

sliders seem to be in a disadvantage compared to the

unknown.

hatching

juveniles

have

been

native pond turtles and even though they are highly adaptive, in this case local conditions likely regulate

Discussion

and contain the invasion.

In Europe, Bulgaria being no exception,

At the Rupite locality (UTM square FL89)

mostly one (rarely two) freshwater turtle species

sliders were encountered regularly and in large

inhabit particular water bodies, thus lowering the

numbers since 1996. The hot mineral water sources

evolutionary drivers for increased competitiveness

there provide suitable conditions. This place is a

over other freshwater turtles. In opposite to the

highly popular tourist destination not only at the local

European water turtles, in the core area of the Pond

level and visitors flow is permanent throughout the

slider’s native distribution it commonly co-occurs

year. The locality is obviously regarded as a very

with various other freshwater turtles, and commonly

suitable place for Pond slider and individuals are

dominates by numbers in local communities. The

likely released constantly.

Pond slider is highly competitive in interspecific

Historically, a large number of sliders were

encounters, both in its native range, as well as in the

released by citizens in an artificial pond within the

range

Sofia Zoo. In this basin, the species has overwintered

requirement such as Chrysemys picta (Schneider,

invasion.

Some

taxa

with

similar

Original Scientific Paper Tzankov et al. 2015

Hyla VOL. 2015., No.1, Str. 18- 27 ISSN: 1848-2007

1783) seem to avoid slider presence and are rare when

semi-aquatic communities and environments. Highly

living in syntopy (Gibbons 1990). Pond sliders have

alarming results were recently obtained in Spain,

been demonstrated to possess a set of advantages that

where an epizootic event caused by blood fluke

allow them to displace the native species (vs. M.

trematodes

leprosa: better thermoregulatory abilities, Polo-Cavia

documented, with lethal effect over a native meta-

et al. 2012; competitive behavior for food resources,

population of E. orbicularis (Iglesias et al. 2015).

Polo-Cavia

Legislative history and impacts

al.

2010;

vs.

orbicularis:

with

North

American

origin

was

competition for basking sites and impact on survival

On 22 December 1997 the European Council

rates, Cadi and Joly 1999, 2004). Pond sliders

implemented an import ban of T. s. elegans into the

potentially have a long-term impact on local

European Union (Regulation (EC) No. 338/97).

communities, living up to 30 years (estimated by

Subsequently, this led to mass importation of the

Gibbons and Semlitsch 1982). They reach sexual

nominate subspecies T. s. scripta. Quite recently both

maturity at 5–7 years of age and at 110–160 mm

subspecies of sliders (scripta and elegans) were

plastron length (Gibbons and Greene 1990), thus

banned for import in EU (Regulation No 578/2013,

allowing for a relatively quick population growth.

followed

Their relatively low age of maturity and higher

regulations do not exist for controlling sliders already

fecundity [within the native range see Cagle (1946);

within the EU, including their sale/re-sale, release to

in Europe see Perez-Santigosa et al. (2008)]

and removal from the wild.

Regulation

888/2014).

Internal

obviously can be recognised as an advantage over the

Although, Bulgaria entered the EU in 2007,

local native species. The sliders are highly mobile and

at present (2015) hatchling T. scripta spp. are still

are capable of moving to other suitable habitats in a

imported (mainly from the Czech Republic, with

vast range – up to 9 km in natural conditions

unknown origin) and are sold in numerous pet shops.

(Gibbons et al. 1990). Thus, these turtles can populate

For example, an illegal import of 600 hatchlings of T.

a large network of waterbodies quickly. The Pond

sliders are opportunistic animals; their diet is rather

confiscated at Sofia airport customs in 2014. The

flexible and includes mostly abundant aquatic

shipment was from Singapore, where a breeding

vegetation and invertebrates in their native range

centre likely exists.

elegans (declared

as aquarium fish)

were

(Parmenter and Avery 1990). Studies in Europe

Quite recently, individual registration of pet

detected overlap of the food spectrums of T. scripta

herpetofauna became mandatory at the Regional

and the native species, but sliders showed the widest

Inspectorates

diet of all investigated species (Pérez-Santigosa et al.

responsible executive bodies. However, there is no

2011).

working mechanism to enforce registration and then

Environment

and

Water,

the

follow it up, e.g. monitoring of what happens with the Sliders host a large set of helminth parasites (Esch et al. 1990) and transmissive pathogens (Bringsøe 2006, Hidalgo-Vila et al. 2008, 2009). Therefore these

sold turtles. According to our observations and unpublished data, in most cases, the turtles are kept until maturity.

animals could be a risk factor for local aquatic and 24

Original Scientific Paper Tzankov et al. 2015

Hyla VOL. 2015., No.1, Str. 18- 27 ISSN: 1848-2007

It seems that the visitors treat the sliders with

Implemented measures and experience from

sympathy and are convinced that they naturally occur

countries facing comparable high risks must be

in Bulgarian wetlands. This attitude promotes a sort

urgently applied to Bulgaria – as Alarcos et al. (2010)

of intentional, but misunderstood and incorrect

pointed

attitude for “release back into the wild” of unwanted

effectiveness and future eradication becomes either

pet turtles. Some owners release the adult animal in a

nearly impossible or very costly.

out,

passive

monitoring

has

limited

nearby water basin – so turtles may appear in urban fountains, ponds, flooded foundations of buildings and puddles; unfortunately, multiple turtles end up in

Acknowledgements We thank Kostadin Andonov, Dimitar

peri-urban and natural habitats. Other owners submit

Chobanov,

turtles to zoos, where they are collected in large

Vladimir Milushev, Vladimir Mladenov, Dimitar

numbers (see above). It is unclear what happens to

Plachiyski for sharing their personal observations.

Krasimir

Donchev,

Erchan

Ersan,

turtles when the capacity of the zoo is filled. Recently, owners have been able to return adult turtles back to the pet shops, which are then sold at the same price as hatchlings.

Possible measures to limit the number and distribution range of Pond sliders in Bulgaria Competent authorities (such as the Regional Inspectorates of Environment and Water and the National Agency for Fisheries and Aqua-culture) should increase their efforts to limit the trade with T. scripta and ban the releases of sliders in the wild (e.g. by organizing campaigns for collecting unwanted pets). Working protocols to follow up on the registered individuals must be implemented. Another urgent measures package is related to the trapping, collecting and removing the Pond sliders from the wild. Proper devices for capture could be funnel traps of various designs, commonly used to sample freshwater turtle populations with very good results (see Plummer 1979, Kennett 1992, Gibbons 1990, Thomas et al. 2008). Additionally, basking traps were efficient for exotic turtle trapping in Spain (PérezSantigosa et al. 2006).

References Alarcos, G.I., Cueto F.F. del, Rodríguez-Pereira A., & Avia M.L. (2010): Distribution records of nonnative terrapins in Castilla and León region (Central Spain). Aquatic Invasions, 5(3): 303-308. Avery, C. & Servan J. (1998): Imminent competition between Trachemys scripta and Emys orbicularis in France. Mertensiella 10: 33–40. Berolero, A. & Canicio A. (2000): Nueva cita de nidificacion en libertad de Trachemys scripta elegans en Cataluna. Boletín de la Asociación Herpetológica Española 11: 84. Bringsøe, H. (2001): Trachemys scripta (Schoepff, 1792) – Buchstaben-Schmuckschildkröte. pp. 525– 583. In: Fritz, U. (Hrsg.) Handbuch der Reptilien und Amphibien Europas, Band 3/IIIA: Schildkröten (Testudines) I. Wiebelsheim (Aula). Bringsøe, H. (2006): NOBANIS – Invasive Alien Species Fact Sheet – Trachemys scripta. Online Database of the North European and Baltic Network on Invasive Alien Species. http://www.nobanis.org Cadi, A. & Joly P. (1999): The introduction of the slider turtle (Trachemys scripta elegans) in Europe: competition for basking sites with the European pond turtle (Emys orbicularis). Chelonii 2: 95–100. Cadi, A. & Joly P. (2004): Impact of the introduction of the red-eared slider (Trachemys scripta elegans) on survival rates of the European Pond Turtle (Emys orbicularis). Biodiversity and Conservation 13: 2511–2518. Cadi, A., Delmas V., Prevot-Julliard A.C., Joly P., Pieau C. & Girondot M. (2004): Successful reproduction of the introduced slider turtle (Trachemys scripta elegans) in the South of France. 25

Hyla VOL. 2015., No.1, Str. 18- 27 ISSN: 1848-2007

Aquatic Conservation: Marine and Freshwater Ecosystems 14: 237–246. Cagle F.R. (1946): The growth of the slider turtle, Pseudemys scripta elegans. Am. Midl. Nat. 36: 685–739. Capalleras, X. & Carretero M.A. (2000): Evidencia de reproduccion con exito en libertad de Trachemys scripta en la Peninsula Iberica. Boletín de la Asociación Herpetológica Española 11: 34–35. Commission Implementing Regulation (EU) No 578/2013 of 17 June 2013 suspending the introduction into the Union of specimens of certain species of wild fauna and flora Official Journal of the European Union, L 169/1. Commission Implementing Regulation (EU) No 888/2014 of 14 August 2014 prohibiting the introduction into the Union of specimens of certain species of wild fauna and flora Official Journal of the European Union, L 243/21. De Roa, E. & Roig J.M. (1997): Puesta en habitat natural de la tortuga de Florida (Trachemys scripta elegans) en Espana. Boletín de la Asociación Herpetológica Española 8: 48–50. Esch, G.W., Marcogliese D.J., Goater T.M. & Jacobson K.C. (1990): Chapter 23. Aspects of the Evolution and Ecology of Helminth Parasites in Turtles: A Review. pp. 299-307. In: J. Whitfield Gibbons (ed.) Life History and Ecology of the Slider Turtle. Smithsonian Institution Press. Washington, D.C. Ferri, V. & Soccini C. (2003): Riproduzione di Trachemys scripta elegans in condizioni seminaturali in lombardia (Italia settentrionale). Natura Bresciana 33: 89–92. Ficetola, G.F., Monti A. & Padoa-Schioppa E. (2003): First record of reproduction of Trachemys scripta in the Po Delta. Museo Civico di Storia Naturale Ferrara 5: 125–128. Gemel, R., Marolt, M. & Ochsenhofer, G. (2005): Ungewöhnliche „Naturbrut“ einer Rotwangen Schmuckschildkröte (Trachemys scripta elegans) in der Südsteiermark. ÖGH-Aktuell, Wien 15: 9–11. Gibbons, J.W. (1990): Chapter 2. Turtle Studies at SREL: A Research Perspective. pp. 19-44. In: J. Whitfield Gibbons (ed.) Life History and Ecology of the Slider Turtle. Smithsonian Institution Press. Washington, D.C. Gibbons, J.W. & Semlitsch R.D. (1982): Survivorship and longevity of a long-lived vertebrate species: How long do turtle live? Journal of Animal Ecology 51: 523–527. Gibbons, J.W. & Greene J. L. (1990): Chapter 9. Reproduction in the Slider and Other Species of Turtles. pp. 124-134. In: J. Whitfield Gibbons (ed.)

Original Scientific Paper Tzankov et al. 2015

Life History and Ecology of the Slider Turtle. Smithsonian Institution Press. Washington, D.C. Gibbons, J.W., Greene J.L. & Congdon J. D. (1990): Chapter 16. Temporal and Spatial Movement Patterns of Sliders and Other Turtles. pp. 201-215. In: J. Whitfield Gibbons (ed.) Life History and Ecology of the Slider Turtle. Smithsonian Institution Press. Washington, D.C. Girondot, M., Delmas V. & Prévot-Julliard A-C. (2012): Nouveles données sur la ponte de la tortue de floride (Trachemys scripta elegans) en Île-deFrance. Bulletin de la Société Herpétologique de France, Paris 142-143: 71–78. Gutleb, B. & Happ. H. (2002) Schildkröten in Kärnten. Carinthia II 192(112): 155–160. Hidalgo-Vila J., Díaz-Paniagua C., Pérez-Santigosa N., de Frutos-Escobar C. & Herrero–Herrero A. (2008): Salmonella in free-living exotic and native trutles and in pet exotic turtles from SW Spain. Research in Veterinary Science 85(3): 449–452. Hidalgo-Vila J., Díaz-Paniagua C., Ribas A., Florencio M., Pérez-Santigosa N. & Casanova J. C. (2009): Helminth communities of the exotic introduced turtle, Trachemys scripta elegans in southwestern Spain: Transmission from native turtles. Research in Veterinary Science 86(3): 463– 465. Iglesias, R., García-Estévez J. M., Ayres C., Acuña A. & Cordero-Rivera A. (2015): First reported outbreak of severe spirorchiidiasis in Emys orbicularis, probably resulting from a parasite spillover event. Diseases of Aquatic Organisms 113: 75-80. Kennett, R. (1992): A new trap design for catching freshwater turtles. Wildlife Research 19: 443–445. Kleewein, A. (2014): Natural reproduction of Trachemys scripta troostii (Holbrook, 1836) x Trachemys scripta scripta (Schoepff, 1792) in Austria. Herpetozoa 26(3/4): 183-185. Martinez-Silvestre, A. (1997): Nota sobre la reproduccion en condiciones naturals de la tortuga de Florida (Trachemys scripta elegans) en Masquefa (Cataluna, España). Boletín de la Asociación Herpetológica Española 8: 40–42. Młynarski, M. (1976): Testudines. In: O. Kuhn (ed.), Encyclopedia of Paleoherpetology, Gustav Fischer Verlag, Stuttgart, New York, Part. Parmenter, R. & Avery H. W. (1990): Chapter 20. The Feeding Ecology of the Slider Turtle. pp. 257266. In: J. Whitfield Gibbons (ed.) Life History and Ecology of the Slider Turtle. Smithsonian Institution Press. Washington, D.C. Pérez-Santigosa, N., Díaz-Paniagua C., Hidalgo-Vila J., Robles F., Pérez de Ayala J.M., Remedios M., 26

Hyla VOL. 2015., No.1, Str. 18- 27 ISSN: 1848-2007

Barroso J.L., Valderrama J., Coronel N., Cobo M.D. & Bañuls S. (2006): Trampas y plataformas de asoleamiento: la major combinación para erradicar galápagos exóticos. Boletín de la Asociación Española de Herpetología 17: 115–120. Pérez-Santigosa, N., Díaz-Paniagua C. & HidalgoVila J. (2008): The reproductive ecology of exotic Trachemys scripta elegans in an invaded area of southern Europe. Aquatic Conservation: Marine and Freshwater Ecosystems 18: 1302–1310. Pérez-Santigosa, N., Florencio M., Hidalgo-Vila J. & Díaz-Paniagua C. (2011): Does the exotic invader turtle, Trachemys scripta elegans, compete for food with coexisting native turtles? Amphibia-Reptilia 32: 167–175. Pleguezuelos J.M. (2004): Las especies introducidas de anfibios y reptiles. 501–532. In: Pleguezuelos J. M., Márquez R., Lizana M. (eds) Atlas y Libro Rojo de los Anfibios y Reptiles de España, Dirección General de la Conservación de la Naturaleza Asociación Herpetológica Española (3a impresión): Madrid. Plummer, M.V. (1979): Collecting and marking. pp. 45–60. In: M. Harless and H. Morlock (eds.) Turtles: Perspectives and Research, John Wiley and Sons, New York. Polo-Cavia, N., López, J. & Martín P. (2010): Aggressive interactions during feeding between native and invasive freshwater turtles. Biological Invasions 13:1387–1396. Polo-Cavia, N. & López, J. & Martín P. (2012): Feeding status and basking requirements of

Original Scientific Paper Tzankov et al. 2015

freshwater turtles in an invasion context. Physiology & Behavior 105: 1208–1213. Sperone, E., Crescente A., Brunelli E., Paolilli G. & Tripepi S. (2010): Sightings and successful reproduction of allochthonous reptiles in Calabria. Acta Herpetologica 5(2): 265–273. Stojanov, A., Tzankov N. & Naumov B. (2011): Die Amphiben und Reptilien Bulgariens. Chimaira, Frankfurt am Main. Stoyanov, A. (2015): Registered high mortality of allochthon Red-eared Sliders (Trachemys scripta elegans) in an artificial pool in Sofia, Bulgaria. HYLA 2015(1): 65–69. Thomas, R. B., Nall I.M. & House W.J. (2008): Relative efficacy of three different baits for trapping pond-dwelling turtles in east-central Kansas. Herpetological Review 39(2): 186–188. Tzankov, N.D., Popgeorgiev G.S., Naumov B.Y., Stoyanov A.Y., Kornilev Y.V., Petrov B.P., Dyugmedzhiev A.V., Vergilov V.S., Draganova R.D., Lukanov S.P. & Westerström A.E. (2014): Identification guide of the amphibians and reptiles in Vitosha Nature Park. Directorate of Vitosha Nature Park, Sofia. Vamberger, M., Lipovšek, G. & Gregorič, M. (2012): First reproduction record of Trachemys scripta (Schoepff, 1792), in Slovenia. Herpetozoa 25(1/2): 76–79. Wüthrich, F. (2004): Naturbruten im Jahr 2003 in der Schweiz. Testudo 13(3): 5–20.

Original Scientific Paper

Hyla VOL. 2015., No.1, Str. 28 - 35

Kleewein 2015

ISSN: 1848-2007

Investigating temperature tolerance in wild broods of Trachemys scripta elegans (Reptilia: Testudines: Emydidae) in Austria Istraživanje temperaturne tolerance u divljim populacijama Trachemys scripta elegans (Reptilia: Testudines: Emydidae) u Austriji ANDREAS KLEEWEIN

University of Vienna, Department of Integrative Zoology, Althanstraße 14, A-1090 Vienna, Austria, andreas.kleewein@gmx.net

Abstract Reproduction of the freshwater chelonian, the red-eared slider, Trachemys scripta elegans (WiedNeuwied, 1836), has been documented numerous times in the wild in Europe. The aim of this work was to show the temperature tolerance in wild broods of T. s. elegans in Austria. In the Austrian province of Carinthia, this allochthonous subspecies displays a huge tolerance regarding clutch temperature. Clutch temperature was measured in half-hour intervals during the entire incubation period of 118 days. The greatest variation in temperature in a single day ranged from 19.3°C to 37.1°C: a shift of 17.8°C. The maximum temperature reached during the entire incubation period was 38.7°C, the minimum temperature was 11.5°C. Average temperature was 22.5°C. Shell dimensions and weight of hatchlings were low. This indicates a negative influence of the extreme temperatures in clutches that are incubated under natural conditions in Austria. Nevertheless, broods in the wild are to be expected much more frequently in Europe than hitherto assumed.

Key words: Reproduction, clutch temperature, temperature variation, incubation period Sažetak Razmnožavanje slatkovodne crvenouhe kornjače, Trachemys scripta elegans (Wied-Nuwied, 1836) u divljini u Europi je već zabilježeno nebrojeno puta. Cilj ovog rada je prikazati temperaturnu tolerancu divljih populacija T. s. elegans u Austriji. Ta alohtona podvrsta pokazuje veliku tolerancu po pitanju temperature legal u pokrajini Koruškoj u Austriji. Temperatura legla je mjerena u 30-minutnim intervalima kroz cijeli period inkubacije od 118 dana. Najveća razlika temperature u pojedinom danu je bila od 19,3°C do 32,1°C: razlika od 17,8°C. Najviša zabilježena temperature je bila 38,7°C, a najniža 11,5°C. Prosječna temperature je bila 22,5°C. Dimenzije oklopa i masa mladunaca su bile male. To ukazuje na nepovoljan utjecaj temperaturnih ekstrema u leglima u austrijskoj prirodi. Unatoč tome, očekuje se povećanje učestalosti legala u Europi nego što je do sada bilo pretpostavljano. Ključne riječi: Razmnožavanje, temperatura legla, temperaturna varijacija, trajanje inkubacije

Original Scientific Paper

Hyla VOL. 2015., No.1, Str. 28 - 35

Kleewein 2015

ISSN: 1848-2007

INTRODUCTION

Temperature measurements were taken

The red-eared slider, Trachemys scripta

using two Tinytag Talk 2 Temperature Loggers

elegans (Wied-Neuwied, 1836), is among the most

(Type TK-4014). One logger was buried at a depth

frequently occurring allochthonous turtle species in

of 12 cm directly by the clutch, in order to measure

the world. The Global Invasive Species Database

the soil temperature. The second logger was

regards it as one of the “100 of the world’s worst

positioned 2 m above the ground, measuring

invasive alien species“ (van Dijk et al. 2013).

outside temperatures. Data recording started on 4

This led to an import ban on the trade of this

June 2012 after oviposition of a female T. s.

species within the European Union in 1997. Reports

elegans, and lasted until 29 September 2012, when

of successful reproduction in the wild in various

the eggs hatched. Daily average temperature and

European countries have confirmed that the species

daily temperature range were calculated between

is able to reproduce outside of its natural range

00:00 and 24:00 h. The measurement interval was

(Girondot et al. 2012, Vamberger et al. 2012,

30 minutes.

Kleewein 2014). The majority of sites with released

Rainfall data was provided by the ZAMG

turtles in Austria have been recorded in the

(Austrian central institution for meteorology and

province of Carinthia. A comprehensive survey

geodynamics). The meteorological station from

revealed 47 bodies of water in which allochthonous

which this data originates is 5 km from the clutch

turtles occur (Kleewein 2007). Reproduction in the

site, also in the Klagenfurt basin (E: 14°19’04”, N:

wild in Carinthia is also already known (Gutleb &

46°38’54”, WGS84 coordinate system; 452 m

Happ 2002, Kleewein 2014).

a.s.l.), and therefore it provides authentic data for

For many years, the Happ reptile zoo in

the study site. Substrate moisture could not be

Klagenfurt has been receiving allochthonous turtles

measured and was estimated subjectively.

that have largely been found in the wild. The zoo

Clutch temperatures of a wild brood of Trachemys

has a dedicated pond for accommodating these

scripta (Kleewein 2014) at Tallach, 17 km to the

animals, providing the turtles with near-natural

south-west (E: 14°04’13”, N: 46°32’20”, WGS84

conditions.

coordinate system; 516 m a.s.l.), are compared and discussed.

MATERIAL AND METHODS The outdoor turtle pond of the Happ reptile

RESULTS

zoo in Klagenfurt was chosen for data acquisition,

On 29 September 2012, a hole measuring

because male and female animals are kept here

2.5 cm in diameter was discovered at the protected

together. Oviposition occurs regularly at an

clutch site, indicating hatching. The wire mesh and

oviposition site made up of an earth-sand mix. The

uppermost layers of earth were removed, revealing

study site is situated in the Klagenfurt basin (E:

a carapace. A live hatchling (hatchling 2) crawled

14°15’56”, N: 46°37’10”, WGS84 coordinate

out of the egg chamber and made its way towards

system; 441 m a.s.l.), which resembles inner-alpine

the pond. Its yolk sac was already completely

areas thermally, but with a continental influence. A

absorbed, and a small part of the plastron was not

wire mesh at the surface with 2.5 x 2.5 cm openings

yet closed. The egg tooth was clearly visible.

provides protection from clutch predators.

Regarding the carapace scutes, the second vertebral one was divided, meaning a total of six vertebral 29

Original Scientific Paper

Hyla VOL. 2015., No.1, Str. 28 - 35

Kleewein 2015

ISSN: 1848-2007

scutes were present. There were 12 marginal and

afternoons between 15:00 and 18:30 h. The

five costal scutes on each side of the carapace. The

minimum temperature measured in the clutch was

plastron, on the other hand, did not show any

11.5°C (7:30 h; 21 September 2012), the lowest

meristic abnormalities (Tab. 1). On 1 October 2012,

temperatures usually being reached in the mornings

between 6:00 and 8:00 h.

second

hatchling

was

discovered

during

maintenance work in the outdoor enclosure – the

The maximum daily temperature range in the clutch

first-hatched young (hatchling 1). Its yolk sac was

was 17.8°C (28 June 2012). In this case, the

not yet fully absorbed, and the animal was

temperature rose from 19.3°C (7:00 h) to 37.1°C

altogether smaller, but did not show any meristic

(17:00 h). The smallest daily temperature range was

abnormalities (Tab. 1). Sex-specific characteristics

2.1°C on a relatively cool day with temperatures

of both hatchlings, such as the cloaca positioned

between 16.3°C (7:30 h) and 18.4°C (16:00 h). The

closer to the end of the tail, indicated that the

average daily temperature range during the entire

hatchlings were males. Measurements of both

incubation period was 10.4°C.

individuals one year after hatching showed that

Out of the 118 days of development, 79% of days

both animals had grown well and had increased in

had a daily average temperature below 25°C (Fig.

weight. Hatchling 1 nevertheless remained well

1). The first third of the development period was

behind hatchling 2 in both size and weight (Tab. 1).

the warmest, with a mean daily temperature of

Three dead individuals in development stages 23,

24.7°C, the second third had a mean daily

25 and 26, according to Greenbaum (2002), were

temperature of 23°C, and the third 19.9°C. The

also found in relative proximity to the surface. The

mean daily temperature during the entire incubation

embryos of all other eggs in deeper parts of the

period,

chamber had died in much earlier development

temperatures, was 22.5°C.

calculated

using

the

daily

average

stages, and were therefore already completely

Rainfall from June to September was 593

decomposed and could not be classified by

mm, the most of which (292.5 mm) fell in July, in

development stage.

the second third of the development period. The

The chamber contained a total of 22 eggs. Due to

months of June (84 mm), August (69.9 mm) and

the proximity of the pond and the high soil water

September (146.6 mm), on the other hand, were

level, 17 of the 22 eggs in this Klagenfurt clutch

very dry (Fig. 1).

were affected by permanent stagnant moisture. Only the uppermost eggs were surrounded by dry incubation substrate. Therefore, only two eggs were able to develop fully and hatch live young. Temperature measurement was conducted over 118 days, and the average incubation period can also be assumed to be around that duration, since the first hatchling had already hatched shortly before this time. The maximum temperature measured in the clutch was 38.7°C (16:30 h; 30 June 2012), the highest daily temperatures always being reached in the 30

Original Scientific Paper

Hyla VOL. 2015., No.1, Str. 28 - 35

Kleewein 2015

ISSN: 1848-2007

gramima (g). HN – broj mladunca, CL – duljina karapaksa, CB – širina karapaksa, PL – duljina plastrona, PB – širina plastrona, SH – visina oklopa. HN CL CB PL PB SH Weight 2012

2.8

2.5

2.6

2.2

1.4

2013

5.5

5.2

4.9

3.9

2.4

2012

3.1

2.9

2.8

2.5

1.6

2013

6.8

6.0

5.9

4.7

2.8

Temperature °C

50 30

20 10

precipitation Max. clutch

Max. air Min. clutch

Precipitation in mm

Table 1. Morphometric data of the two Trachemys scripta elegans hatched in Klagenfurt (Carinthia, Austria) in 2012, and one year after hatching. Shell measurements in centimetres (cm), body mass in gram (g). HN - Hatchling Number, CL Carapace length, CB - Carapace breadth, PL Plastron length, PB - Plastron breadth, SH - Shell Height Tablica 1. Morfometrijski podatci dvije jedinke Trachemys scripta elegans koje su se izlegle u Klagenfurtu (Karintija, Austrija) 2012. godine, i jednu godinu nakon izlijeganja. Mjere na oklopu izražene su u centimetrima (cm) a tjelesna masa u

Min. air

Figure 1. Outside temperature and rainfall data from the clutch site in Klagenfurt. Daily maximum and minimum outdoor temperature were measured 2 m above ground, maximum and minimum ground temperature were measured at a depth of 12 cm. Rainfall data refers to the period from the beginning of June to the end of September. Slika 1. Podatci o vanjskim temperaturama i padalinama zbilježenim za leglo u Klagenfurtu. Dnevni maksimum i minimum su mjereni na 2 m iznad zemlje a dnevni maksimum i minimum temperature tla su mjereni na dubini od 12 cm. Podatci o padalinama se odnose na period od početka lipnja do kraja rujna.

Original Scientific Paper

Hyla VOL. 2015., No.1, Str. 28 - 35

Kleewein 2015

ISSN: 1848-2007

Temperature °C

50 40 30 20 10 0 4.6.2012

4.7.2012 Max. clutch K

4.8.2012 Min. clutch K

4.9.2012 Max. clutch T

4.10.2012 Min. clutch T

Figure 2. Comparison of maximum and minimum ground temperatures between the clutches in Klagenfurt (K) and Tallach (T). Temperatures in Klagenfurt were measured at a depth of 12 cm, in Tallach at 10 cm. Minimum temperatures of both clutches are almost identical, the maximum temperatures in Klagenfurt are much higher. Slika 2. Usporedba maksimuma i minimuma temperature tla između legal u Klagenfurtu (K) i Tallachu (T). Temperature u Klagenfurtu su mjerene na dubini od 12 cm, a u Tallachu na dubini od 10 cm. Minimalne temperature oba legla su skoro identične, dok su maksimalne temperature u Klagenfurtu značajno veće.

DISCUSSION

during incubation, this can kill the embryos (Tucker

Survival rate and development of embryos

et al. 1997). This was also the case at the deeper

in eggs with flexible, porous shells – as is the case

part of the clutch at the Klagenfurt site. The

in T. s. elegans – are strongly influenced by the

combination of the high groundwater level and

moisture of the incubation substrate, due to the

waterlogged soil caused the embryos in deeper parts

increased exchange between the egg and its

of the chamber to die.

surroundings (Congdon & Gibbons 1990). In dryer

Average incubation period is dependent on

substrates, hatchlings are generally smaller and

temperature and lasts 112.5 days under laboratory

lighter (Congdon & Gibbons 1990). This was also

conditions at an average temperature below 25°C,

evident in the two uppermost eggs from the

according to

Klagenfurt clutch which hatched live. These two

development period of 118 days and the low

hatchlings, which had a body mass of 5 and 6 g

incubation temperature measured in Klagenfurt

respectively, thereby lying at the lower end of the

match these laboratory results. Under natural

range of the body mass of wild hatchlings in North

conditions in their native habitat, the young hatch

America (4.4-10.3 g; mean 8.2 g; n=151) (Tucker

after 60-80 days (Ewert 1979). The Tallach clutch

2000). The Tallach hatchlings had only between 5

also had a long incubation period of 119 days

and 6 g and the incubation substrate was dry

(Kleewein 2014) (Fig. 2). This shows that

(Kleewein 2014).

incubation periods under natural conditions in

On the one hand, moist substrate promotes an

Austria are longer by one half to one third than

increase in embryonic mass; on the other hand,

incubation periods in the species’ native North

eggs in moist substrate require a longer incubation

American habitat. Furthermore, the possibility of

period than eggs in drier substrate (Tucker &

successful reproduction despite low incubation

Paukstis 1999). If moisture levels are too high

temperatures and huge temperature variation could

Ernst

Lovich (2009).

The

Original Scientific Paper

Hyla VOL. 2015., No.1, Str. 28 - 35

Kleewein 2015

ISSN: 1848-2007

be proven. Ewert & Nelson (1991) describe the

Generally, there would be enough habitats available

development of males at 22.5, 25 or 27°C, and the

around the eastern Alps that could allow the

development of females at 30°C. The transitional

development of hatchlings.

range of temperatures under stable laboratory

T. scripta can reproduce for the first time around

conditions lies between 29.0 and 29.5°C (Bull et al.

the age of eight years on average (Gibbons et al.

1982, Paukstis & Janzen 1990). Cadi et al. (2004)

1981), and at this age their body mass is still

state a transitional range of temperatures between

smaller than that of adults. Compared to adult

28.30°C and 30.61°C, at which both sexes can

animals, however, the young are subject to much

develop equally. The most decisive phase for the

greater predation pressure, especially from raptors

maturing T. scripta embryo is the middle third of

and corvids, as well as from carnivorous mammals

the incubation period. It is only after this time that

such as foxes. What is more, even in South

the sexual organs begin to differentiate, lasting until

Carolina, only 10% of a population reach the age of

the onset of sex-specific gonadal morphogenesis

ten years, and only 1% of turtles reach 20 years

(Wibbels et al. 1991). In the Klagenfurt case, clutch

(Gibbons 1987). For these reasons, only a small

temperature dropped constantly from oviposition to

number of hatchlings could be expected to reach

hatching, the mean daily temperature already being

maturity in Austria.

below 25°C in the first third of development. In

Long, harsh frosts reduce the hatching rate,

Tallach, at an overall average temperature of

body temperatures below 0°C down to -4°C are

21.4°C, it was also only males that hatched. Due to

tolerated only for a few hours (Churchill & Storey

the low recorded average incubation temperatures,

1992). Slider hatchlings of the northern North

it is currently not possible for females to develop in

American populations generally overwinter in the

Austrian clutches in the wild.

nest, and react sensitively to temperatures around

The maximum daily range of temperature

-0.6°C-4.0°C (Packard et al. 1997, Tucker &

in a Trachemys scripta troostii (Holbrook, 1836)

Packard 1998, Costanzo et al. 2008). An analysis of

clutch in Tennessee was 8°C (Cagle 1937). For

soil temperatures during the course of one year,

comparison’s sake, the average daily range of

measured at the hatching site in Klagenfurt from the

temperature in a 10.7 cm deep clutch of Chrysemys

winter of 2011 to the winter of 2012, showed

picta (Schneider, 1783) was 7°C (Refsnider et al.

minimum temperatures reaching -3.5°C, which

2013). With 10.4°C at a depth of 12 cm, the

would have had a detrimental effect on survival rate

measurements in Klagenfurt revealed only a

in any overwintering clutch.

slightly higher average daily range of temperature;

One year, or a few years, with low reproductive

but they indicated a much greater tolerance

success will not lead to the extinction of

regarding the maximum daily range of temperature,

populations. What is more decisive for the

with 17.8°C. Since substrate moisture and clutch

geographic range and persistence of a population is

temperature are decisive for development of the

the long-term average temperature (Rödder et al.

embryos, and as these values were considerably

2009). Due to the low clutch temperatures

lower in Carinthia than in the species’ native

measured in Carinthia, only males are able to

habitat, this shows that the species possesses

develop at the moment. This can, however, provide

considerable tolerance regarding temperature in

the basis for future reproductions in certain bodies

central European climates. 33

Hyla VOL. 2015., No.1, Str. 28 - 35 ISSN: 1848-2007

of water that already contain released, sexually mature females.

REFERENCES Bull, J.J., Vogt, R.C. & McCoy, C.J. (1982): Sex determining temperatures in turtles: a geographic comparison. Evolution 36: 326-332. Cadi, A., Delmas, V., Prévot-Julliard, A.-C., Joly, P., Pieau, C. & Girondot, M. (2004): Successful reproduction of the introduced slider turtle (Trachemys scripta elegans) in the South of France. Aquatic Conservation: Marine and Freshwater Ecosystems 14: 237-246. Cagle, F.R. (1937): Egg laying habits of the slider turtle (Pseudemys troostii), the painted turtle (Chrysemys picta), and the musk turtle (Sternotherus odoratus). Journal of the Tennessee Academy of Science 12: 87-95. Churchill, T.A. & Storey, K.B. (1992): Responses of freezing exposure of hatchling turtles Trachemys scripta elegans: factors influencing the development of freeze tolerance by reptiles. Journal of Experimental Biology 167: 221-233. Congdon, J.D. & Gibbons, J.W. (1990): Turtle Eggs: Their Ecology and Evolution. pp. 109-123. In Gibbons, J.W. (ed.) Life History and Ecology of the Slider Turtle. Smithsonian Institution Press. Costanzo, J.P., Lee Jr., R.E. & Ultsch, G.R. (2008): Physiological ecology of overwintering in hatchling turtles. Journal of Experimental Zoology 309A: 297-379. van Dijk, P.P., Harding, J. & Hammerson, G.A. (2013): Trachemys scripta. The IUCN Red List of Threatened Species. Version 2014.3. <www.iucnredlist.org>. Downloaded on 22 May 2015. http://www.iucnredlist.org/details/22028/0. Ernst, C.H. & Lovich, J.E. (2009): Turtles of the United States and Canada. Second Edition. John Hopkins University Press, Baltimore. Ewert, M.A. (1979): The embryo and its egg: Development and natural history. pp. 333-413. In Harless, M., Morlock, H. (eds.) Turtles: Perspectives and research. John Wiley and Sons. Ewert, M.A. & Nelson, C.E. (1991): Sex determination in turtles: Diverse patterns and some possible adaptive values. Copeia 1991: 5069. Gibbons, J.W. (1987): Why do turtles live so long? Bioscience 37: 262-269. Gibbons, J.W., Semlitsch, R.D., Greene, J.L. & Schubauer, J.P. (1981): Variation in age and size at maturity of the Slider turtle (Pseudemys scripta). The American Naturalist 117: 841-845. Girondot, M., Delmas, V. & Prévot-Julliard, A.-C. (2012): Nouveles données sur la ponte de la tortue de Floride (Trachemys scripta elegans) en Île-deFrance. Bulletin de la Société Herpétologique de France 142-143: 71-78.

Original Scientific Paper Kleewein 2015

Greenbaum, E. (2002): A standardized series of embryonic stages for the emydid turtle Trachemys scripta. Canadian Journal of Zoology 80: 13501370. Gutleb, B. & Happ, H. (2002): Schildkröten in Kärnten. Carinthia II 192/112: 155-160. Kleewein, A. (2007): Verbreitung der RotwangenSchmuckschildkröte (Trachemys scripta elegans) in Kärnten. Carinthia II 197/117: 53-58. Kleewein, A. (2014): First record of reproduction in open land of Trachemys scripta troostii (Holbrook, 1836) with the nominate species Trachemys scripta (Schoepff, 1792) in Austria. Herpetozoa 26: 183-185. Packard, G.C., Tucker, J.K., Nicholson, D. & Packard, M.J. (1997): Cold tolerance in hatchling Slider turtles (Trachemys scripta). Copeia 1997: 339-345. Paukstis, G.L. & Janzen, F.J. (1990): Sex determination in reptiles: summary of effects of constant temperatures of incubation on sex ratios of offspring. Smithsonian Herpetological Information Service 83: 1-28. Refsnider, J.M., Bodensteiner, B.L., Reneker, J.L. & Janzen, F.J. (2013): Nest depth may not compensate for sex ratio skews caused by climate change in turtles. Animal Conservation 16: 481490. Rödder, D., Kwet, A. & Lötters, S. (2009): Translating natural history into geographic space: a macroecological perspective on the North American Slider, Trachemys scripta (Reptilia, Cryptodira, Emydidae). Journal of Natural History 43: 2525-2536. Tucker, J.K. (2000): Annual variation in hatchling size in the red-eared slider turtle (Trachemys scripta elegans). Herpetologica 56: 8-13. Tucker, J.K., Janzen, F.J. & Paukstis, G.L. (1997): Response of embryos of the red-eared turtle (Trachemys scripta elegans) to experimental exposure to water-saturated substances. Chelonian Conservation and Biology 2: 345-351. Tucker, J.K. & Packard, G.C. (1998): Overwinter survival by hatchling sliders (Trachemys scripta) in West-Central Illinois. Journal of Herpetology 32: 431-434. Tucker, J.K. & Paukstis, G.L. (1999): Post-hatching substrate moisture and overwintering hatchling turtles. Journal of Herpetology 33: 608-615. Vamberger, M., Lipovšek & G., Gregorič, M. (2012): First reproduction record of Trachemys scripta (Schoepf, 1792), in Slovenia. Herpetozoa 25: 76-79. Wibbels, T., Bull, J.J. & Crews, D. (1991): Chronology and morphology of temperaturedependent sex determination. Journal of Experimental Zoology 260: 371-381.

Hyla VOL. 2015., No.1, Str. 28 - 35

Original Scientific Paper Kleewein 2015

ISSN: 1848-2007

ACKNOWLEDGEMENTS

for Integrative Zoology, especially to Walter Hรถdl,

I would like to thank Helga Happ, of the Happ

for material and professional support.

reptile zoo, for the possibility to conduct this study in her zoo. Thanks are also due to the Department

Hyla

VOL. 2015., No.1, Str. 36- 43 ISSN: 1848-2007

Original Scientific Paper Dimaki et al. 2015

New data on the distribution and population density of the African Chameleon, Chamaeleo africanus and the Common Chameleon, Chamaeleo chamaeleon in Greece Novi podatci o distribuciji i populacijskoj gustoći afričkog kamelenona, Chamaeleo africanus i običnog kameleona, Chamaeleo chamaeleo u Grčkoj MARIA DIMAKI1*, BASIL CHONDROPOULOS2, ANASTASIOS LEGAKIS3, EFSTRATIOS VALAKOS4, MARIOS VERGETOPOULOS1 1

Goulandris Natural History Museum, 100 Othonos St., 145 62 Kifissia, Greece, mdim@gnhm.gr 2 Section of Animal Biology, Dept. of Biology, Univ. of Patra, Greece. 3 Zoological Museum, Dept. of Biology, Univ. of Athens, Greece. 4 Section of Animal & Human Physiology, Dept. of Biology, Univ. of Athens, Greece.

Abstract New data on the distribution and the population density of the Common Chameleon Chamaeleo chamaeleon (Linnaeus, 1758) and the African Chameleon Chamaeleo africanus Laurenti, 1768 are reported from Greece. The data for the Common Chameleon was collected from Samos Island (Aegean Sea) and for the African Chameleon from the SW Peloponnese. The period of the data collection is from 1998 till 2014. The African Chameleon is an allochthonous species for Greece and its presence in the area of Gialova Pylos is likely due to its introduction in historical times, because chameleons were often used in the past as pets by people and kings (Bodson, 1984). Some months ago a new population of the Common Chameleon was discovered in Attica. The distribution of the African Chameleon has expanded in the western Peloponnese with at least two new populations. This expansion is due to the local translocation of the species by humans. The population density of the African Chameleon ranged from 0.44 (in 2014) to 401.30 (in 1999) individuals/ha, while for the Common Chameleon ranged from 0.83 (in 2001) to 53,33 ind/ha (in 1998). The mean population density of the African Chameleon in Pylos was 9.69 ind/ha (estimated without the extreme value of 401.30), while that of the Common Chameleon in Samos was 5.26 ind/ha. No statistically significant difference was found in the sex ratio for either chameleon species. Only in the African Chameleon we did find a statistically significant difference between juvenile and adult numbers, as juveniles were more numerous (60.7% of the population). Key words: Chamaeleo africanus, Chamaeleo chameleon, Greece; distribution, population density.

Sažetak Novi podaci o rasprostranjenosti i gustoći populacije običnog kameleona Chamaeleo chamaeleon (Linnaeus, 1758) i afričkog kameleona Chamaeleo africanus Laurenti, 1768 su iznešeni. Podaci za C. chamaeleon su sakupljani na otoku Samos (Egejsko more), a za C. africanus na JZ Peloponezu. Sakupljanje podataka je trajalo od 1998. do 2014. Afrički kameleon je unešena vrsta u Grčkoj, prisutna na području Gialova Pylos i vrlo vjerojatno je unešena davno, jer su kameleoni često uzimani za ljubimce, pogotovo od monarha (Bodson, 1984). Nova vrsta običnog kameleona je otkrivena u Atici pred nekoliko mjeseci. Afrički kameleon se proširio na zapadni Peloponez, gdje tvori bar dvije nove populacije. To je vjerojatno zbog lokalne translokacije od strane ljudi. Gustoća populacije afričkog kameleona se kretala od 0,44 (2014.) do 401,30 (1999.) jedinki/ha, a za

Original Scientific Paper

Hyla

VOL. 2015., No.1, Str. 36- 43 ISSN: 1848-2007

Dimaki et al. 2015

običnog od 0,83 (2001.) do 53,33 (1998.) jed./ha. Srednja gustoća populacije u Pylosu je bila 9,69 jed./ha (procijenjeno bez ekstremne vrijednosti od 401,30 jed./ha) za afričkog, odnosno na Samosu 5,26 jed./ha za običnog kameleona. Nije pronađena statistički značajna razlika u omjeru spolova za obje vrste. Statistički značajna razlika između brojnosti juvenilnih i odraslih jedinki je uočena samo kod afričkih, s time da su juvenilne jedinke bile brojnije (60,7 % populacije). Ključne riječi: Chamaeleo africanus, Chamaeleo chameleon, Grčka; distribucija, gustoča populacije

in the west Peloponnese. The total area in which the

INTRODUCTION The distribution of the Common Chameleon in

chameleons were found in the Peloponnese is about

Greece includes the Aegean islands of Samos, Chios

30 ha (Dimaki 2008). Twelve ha of this area consist

and Crete (Ondrias 1968, Chondropoulos 1986,

of flooded land, meadows that have no vegetation

Dimaki 2008), while the African Chameleon had

during the summer, and roads, so the size of the

been observed only at Gialova near Pylos, in the

suitable habitat for the African Chameleon is 18 ha

southwestern Peloponnese (Böhme et al. 1998,

(Dimaki 2008). In 2013 and 2014 we looked for

Dimaki 2008). Both species are rare in Greece. The

African Chameleons further north of the known

Common Chameleon is listed in the Annex II of the

distribution of the species in the Peloponnese in case

Bern convention, in the Annex IV of the EU Habitats

we could find any new population of the species.

Directive and is also protected by the Greek Law

Samos is 47700 ha, 21.4% of the island consists of

(Presidential Decree 67/1981). The Greek Red Data

pine woods, 40.5% is pastures and 3.6% is villages

Book of Threatened Vertebrates refers to it as an

and roads (Dimitropoulos et al. 1998), so 65.5% of

“Endangered” taxon and to the African Chameleon as

Samos is unsuitable habitat for chameleons. Only

“Critically Endangered”. The genus is listed in the

16450 ha are optimum habitat for the Common

Annex

Basic

Chameleon. After a big fire in July 2000 the optimum

information (such as population size and density) is

habitat was diminished considerably. For August

especially

2000 and September 2001 we estimate the total

the

needed

CITES

for

the

Convention.

conservation

and

management of these threatened species.

habitat of the species about 12720 ha (Dimaki 2008).

In this paper we report basic information

The population size was estimated using the capture-

about the population of both species in Greece.

marking-recapture and the line transect method

Information includes density of the population, and

(Pianka

new data on the distribution of the African

estimation) and Petersen indices were used for

Chameleon. Available information for both species

population estimation. The animals were marked

exists in the PhD thesis of the first author. For the

using waterproof ink, as done by Cuadrado & Loman

Common Chameleon there is more information on the

(1997) and Cuadrado (2001) with the Common

populations in southern Spain (Cuadrado & Santos

Chameleon in Spain and by Dimaki (2008) in Greece.

1997, Cuadrado 1998, 2001).

The animals were handled with care and no animal

1970).

The

Schnabel

(Schumacher

was hurt during the study. MATERIALS AND METHODS

Using the line transect method we recorded

Field work on the Common Chameleon took

individuals identified in the transect, the boundaries

place on Samos island and on the African Chameleon

of which are located on either side of the route that is

Original Scientific Paper

Hyla

VOL. 2015., No.1, Str. 36- 43 ISSN: 1848-2007

Dimaki et al. 2015

chosen by the researcher. The distances traveled were

necessary to catch the animal and it was difficult to

measured by pedometer.

observe the sex – such as when the animal was very

Our estimation of the total population of the species

high on a tree - we did not sex them).

was based on the methodology of Nilson et al. (1999).

From that total 352 were recaptures. No statistically

Data was collected from Samos in June 1998, July

significant difference was found in the sex ratio of the

1999, May, July, August-September 2000, September

species (Mann-Whitney U test, U= 51.0 P=0.53).

2001, August 2010, and August 2014. The exact dates of sampling are given in Table 2. Data from Pylos was collected in April and May 1998, June 1999, May 2000, April 2001, June and August 2003, August-September 2011, August 2013, May and August 2014. The exact dates of sampling are given in Table 1.

Age ratio varied significantly in this species with more juveniles (immature specimens) than adults (Mann-Whitney U test, U= 17.00 P<0.05). We used data of 902 African Chameleons to check the age ratio. Of these individuals, only 164 were adults (39.3 %) (18.8%) and 738 were juveniles (60.7 %) (81.2 %) (SVL < 114 mm).

Sex identification was based on the presence of the hemipenes at the base of the tail of the males. For the African Chameleons we also used the presence of spurs at the hind legs of the males. Age identification was based on the length of the

We captured a total of 125 individuals of the Common Chameleon (30 males, 31 females and 64 of unknown sex). Of these, only 17 were recaptures. Because of the small number of animals that were

body; individuals of the African Chameleon of SVL ≥

found on Samos at each sampling, we could not use

114 mm and of the Common Chameleon of SVL ≥ 84

the capture-marking-recapture method. Instead we

mm are considered adults (Dimaki 2008).

used mainly the transect method.

Using Mann-Whitney U test we compared the ratio of the two sexes as well as that of adult to juveniles. Juveniles were considered African Chameleons of SVL < 114 mm and Common Chameleons of SVL < 84 mm. Newborns were excluded, we also used the measurements of each chameleon only once in case of a recapture.

Thirty-seven

chameleons

were

adults

(55.4%) and 30 juveniles (44.6%). No statistically significant difference was found in the sex ratio (Mann-Whitney U test, U= 15.00 P=0.63), nor in the age ratios of the Common Chameleon (MannWhitney U test, U= 15.50 P=0.68). The population density of the African Chameleon in Pylos and of the Common Chameleon in Samos at

RESULTS We counted a total of 1150 African Chameleons during field work (395 males, 492

each sampling area and period are presented in Tables 1 and 2. Our estimation of the total population of the species is presented in Table 3.

females and 263 of unknown sex). (When it was not

Original Scientific Paper

Hyla

VOL. 2015., No.1, Str. 36- 43 ISSN: 1848-2007

Dimaki et al. 2015

Table 1. Population density of the African Chameleon in Pylos. Tablica 1. Gustoća populacije afričkog kameleona u Pylosu. Date

Sampling area

Population

(ha)

estimation

13-15/4/1998

8.42

14/4/1998

5.5

14.00

15-17/5/1998

13.37

16/5/1998

6.00

Transect

14/5/1998

4.5

7.33

Transect

8-10/6/1999

117

16.76

100.90-140.21

Schnabel

30/6-2/7/1999

0.2

401.30

55.44-143.69

Schnabel

8-10/5/2000

11.31

75.79-82.80

Schnabel

7/4/2001

5.5

3.09

8-10/4/2001

160

22.83

110.64-287.72

Schnabel

5-7/6/2003

9.00

43.09-92.60

Schnabel

5-7/8/2003

6.90

32.37-73.86

Schnabel

30/8-1/9/2011

4.5

53.34-124.91

Schnabel

2-4/9/2011

27.14- 53.57

Schnabel

15-17/8/2013

4.5

20.3

64.57-133.80

Schnabel

3/5/2014

4.5

4.44

Transect

4/5/2014

2.7

1.85

Transect

12/5/2014

4.5

3.56

Transect

25/8/2014

0.6

21.67

Transect

25/8/2014

4.5

Transect

26/8/2014

2.8

Transect

26/8/2014

4.5

0.44

Transect

27/8/2014

2.7

3.70

Transect

27/8/2014

0.6

16.67

Transect

MEAN MEAN

density/ha 95% confidence limits

49.56-78.67

Method

Petersen Transect

79.87-120.90

Petersen

Transect

26.01 without

401.3

9.69

Table 2. Population density of the Common Chameleon in Samos (*: data from Tsapras, 2012). Tablica 2. Gustoća populacije običnog kameleona na Samosu (*: podatci iz Tsapras, 2012). Date Sampling area Population density/ha 95% Method (ha) estimation confidence limits 1-3/6/1998

0.075

4.0

53.33

Transect

19/7/1999

0.95

3.0

3.16

Transect

20/7/1999

1.2

3.0

2.50

Transect

21/7/1999

1.96

5.0

2.55

Transect

Original Scientific Paper

Hyla

VOL. 2015., No.1, Str. 36- 43 ISSN: 1848-2007

Dimaki et al. 2015

22/7/1999

0.95

1.0

1.05

Transect

20-22/5/00

1.2

2.0

1.67

22/5/2000

0.95

2.0

2.11

Transect

3/7/2000

1.96

5.0

2.55

Transect

4/7/2000

1.96

2.0

1.02

Transect

5/7/2000

1.2

1.0

0.83

Transect

6/7/2000

1.96

2.0

1.02

Transect

7/7/2000

1.2

1.0

0.83

Transect

8/7/2000

1.96

3.0

1.53

Transect

26/8/2000

1.96

4.0

2.04

Transect

26/8/2000

1.2

2.0

1.67

Transect

28/8/2000

0.95

5.0

5.26

Transect

31/8/2000

0.95

2.0

2.11

Transect

1/9/2000

0.95

6.0

6.32

Transect

2-2

Schnabel

2/9/2000

1.96

2.0

1.02

Transect

25/9/2001

0.95

4.0

4.21

Transect

26/9/2001

1.96

6.0

3.06

Transect

27/9/2001

1.2

1.0

0.83

Transect

13-14/8/2010

1.05

11.43

2.81-13.78

Schnabel

18-20/10/10*

2.4

3.33

0.99-9.78

Schnabel

21-23/10/10*

1.05

22.86

5.00-35.14

Schnabel

1/8/2014

0.48

2.08

Transect

2/8/2014

2.4

1.67

Transect

MEAN

5.26

Table 3. Estimated total number of the African Chameleon in Pylos (30 ha) and of the Common Chameleon in Samos (47 700ha). Tablica 3. Procjenjeni broj afriÄ?kih kameleona u Pylosu (30 ha) i obiÄ?nog kameleona na Samosu (47 700ha). Date April 1998

Total population of Ch. africanus 196

May 1998

175

June 1999

301

July 1999 May 2000

Total population of Ch. chamaeleon

40000 203

30600

July 2000

31200

August 2000

37100

April 2001

255

September 2001

34000

June 2003

162

August 2003

124

August 2010

145000

Original Scientific Paper

Hyla

VOL. 2015., No.1, Str. 36- 43 ISSN: 1848-2007

Dimaki et al. 2015

October 2010

166000

August - September 2011

216

August 2013

365

May 2014

August 2014

149

23914

During 2013 and 2014 we searched for new

species has expanded its distribution from the village

locations in the Peloponnese for African Chameleons.

of Gialova to the coastline of Romanos village. This

We found two new populations in the western

happened after the introduction of individuals to

Peloponnese (exact localities are not given due to the

Voidokilia

high incidence of illegal collection of the species in

communication).

Greece). The first population is in the NATURA2000

Recently a

site GR2330005 and the second in the NATURA2000

Chameleon was discovered in Attica. This is also an

site GR2320001. The first population was monitored

introduced population that needs to be studied.

the

same

people

new population of the

(personal

Common

during 2013 and 2014. Both adults and newborns were found there. The second population was found

We estimated the population density of the

in the summer of 2014 and we do not know the exact

African Chameleon only by the 2013 known

situation of this population because only three

distribution of the species, without including the new

newborns were found there.

regions, in order to compare the data with those since

Also we found that the species has expanded its

1998. The population density of the African

distribution north-west of its known distribution in

Chameleon was much larger than that of the Common

Gialova. The new distribution of the species in the

Chameleon. A possible explanation is that habitats

Pylos area is from the village of Gialova to the

were very different between sites: wetlands in Pylos

coastline of Romanos village.

vs. rocky and sandy areas in Samos (Rhizos 1998).

In December 2014 a new population of the Common

This difference could determine for instance, a) great

Chameleon was discovered, by the first author, in

differences in food availability between sites, b)

Attica. Because this is a new discovery we know

different

neither the exact distribution nor the population

different soil humidity and hence, a different

density of this introduced population.

reproductive success (Martin 1992), and c) high

microhabitat

conditions

influencing

differences in nesting sites. DISCUSSION

The range of the population density of the African Chameleon was 0.44-401.30 ind. per ha. The

The area of Gialova is the only place that

remarkably high density recorded was in one

was known for the distribution of the African

particular area (and only one year), especially

Chameleon in Greece. The distribution of the African

favourable for the animals. Differences like these are

Chameleon has expanded to the western Peloponnese

not unexpected and have been noted in other

with at least two new populations. This expansion is

chameleon species (Burrage 1973). For Chamaeleo

due to the introduction of the species by people who

namaquensis the population density was 0.5-23.4

like chameleons without any permit or any other legal

(mean 12.8), and for Bradypodion pumilum 8-90 ind

permission (personal communication). Also the

/ha in southwest Africa (Burrage 1973).

Original Scientific Paper

Hyla

VOL. 2015., No.1, Str. 36- 43 ISSN: 1848-2007

Dimaki et al. 2015

For Common Chameleons,

the range of the

error or a difference in behaviour between the sexes

population density was much smaller in Samos than

(Turner 1977)

in Cádiz (south Spain) where the estimation was 20-

In Gialova, juveniles were more numerous than

25 ind/ha (with a maximum of 30 ind/ha (Cuadrado &

adults, with the exception of August 1997, 1998, and

Rodriguez 1997, Cuadrado 1998). These differences

2003. In all other surveys, the juveniles ranged from

could be explained by differences in food availability,

56.0% (in June 1998) to (97.8% in April 200) of the

or the competition between species (Turner 1977,

population. In Samos such a difference was not

Avery 1980).

observed. This might mean that the African

The total population of the African Chameleon for the

Chameleon had larger reproductive success.

period 1998-2014 ranged from 59 to 365 individuals, while the total population of the Common Chameleon in Samos for the period 1999-2014 ranged from 23914 to 166000 individuals. The prospective range in the population can be large over the total sampling period, as according to Turner (1977), lizard populations are not stable during each year, but their density changes. In early spring a high number of the chameleons

are

still

hibernating

(personal

observations), so it is possible that this is the reason that the population seems smaller in spring than in July and August. After the big fire in Samos, the population of the Common Chameleon seemed larger. This might happen because the chameleons are concentrating in optimum habitat, after the reduction of their former habitat. August and September are favourable months for observing chameleons because they mate and thus they move a lot and do not hide themselves in dense vegetation during the night. Furthermore, in these months eggs are hatching, so generally more chameleons are observed. No difference was found in the sex ratio of either species. This is predictable for most lizard species (Burrage 1973). However, in Furcifer pardalis (Bourgat 1968) and in the Common Chameleon from Spain (Blasco 1978) males were more numerous than females. These differences could be due to sampling

REFERENCES Avery, R.A. (1980): Ecophysiology and behaviour of lacertid lizards - towards a synoptic model. Proceedings of the European Herpetological Symposium CWLP, Oxford. 71-73. Blasco, M. (1978): Situacion actual del camaleón común, Chamaeleo chamaeleon L., en la Procincia de Cadiz, España. Boletin de la estacion central de Ecologia. 7(13): 87-90. Böhme, W. & Bonetti, A. & Chiras, G. (1998): The chameleons of the Greek mainland: taxonomic allocation and conservation needs of a second European species (Squamata: Sauria: Chamaeleonidae). Herpetozoa 11 (1/2): 87-91. Bodson, L. (1984). Living reptiles in captivity: a historical survey from the origins to the end of the XVIIIth century. ACTA Zoologica et Pathologica Antverpiensia. 78 (1): 15-32. Bourgat, R. (1968): Etude des variations annuelles de la densite de population de Chamaeleo pardalis Cuv., 1892, dans son biotope de l' ile de la Reunion. Vie Milieu. (C) 19: 227-231. Burrage, B.R. (1973): Comparative ecology and behavior of Chamaeleo pumilus pumilus (Gmelin) and C. namaquensis A. Smith (Sauria: Chamaeleonidae). Annals of the South African Museum 61: 1-158. Chondropoulos, B.P. (1986): A checklist of the Greek reptiles. I. The lizards. Amphibia & Reptilia 7: 217235. Cuadrado, M. (1998): The use of yellow spot colors as a sexual receptivity signal in females of Chamaeleo chamaeleon. Herpetologica. 54 (3): 395-402. Cuadrado, M. (2001): Mate guarding and social mating system in male common chameleons (Chamaeleo chamaeleon). Journal of Zoology. 255: 425-435. Cuadrado, M. & Loman, J. (1997): Mating behaviour in a Chameleon (Chamaeleo chamaeleon) population in southern Spain - effects of male and female size. Herpetologia Bonnensis. Böhme, W., Bischoff, W & Ziegler (Eds). 1997: 81-88

Original Scientific Paper

Hyla

VOL. 2015., No.1, Str. 36- 43 ISSN: 1848-2007

Cuadrado, M. & Santos, M.R. (1997): Distribucion actual del camaleón en la peninsula Iberica. Quercus. 133: 31-36. Dimaki, M. (2008): Ecology and physiology of chameleons (Chamaeleo spp.) in Greece (PhD thesis) University of Athens, (in Greek) 202 pages. Dimitropoulos, A. & Dimaki, M. & Ioannidis Y. (1998): The fauna of Samos. (Ed.) “N. Dimitriou” foundation. 13:180 pages. Martin, J. (1992): Chameleons: Nature’s Masters of Disguise. Blandford (Ed). UK. Pages: 176. Nilson, G. & Andrén C. & Ioannidis, Y. & Dimaki, M. (1999): Ecology and conservation of the Milos viper, Macrovipera schweizeri (Werner, 1935). Amphibia & Reptilia. 20: 355-375. Ondrias, J.C. (1968): Liste des amphibiens et des reptiles de la Grece. Biologia Gallo-Hellenica I (2):111-135. Pianka, E.R. (1970): Comparative autecology of the lizard Cnemidophorus tigris in different parts of its geographic range. Ecology. 51: 703-720. Rhizos, S. (1998): Geology of Samos island. In: The fauna of Samos. (Ed.) “N. Dimitriou” Foundation. 13: 29-32. Tsapras, P. (2012). Population estimation and ecological characteristics of the Common Chameleon (Chamaeleo chamaeleon) in two areas of Samos island, Greece. In Greek with English summary. pp 69. Turner, F.B. (1977): The dynamics of populatons of Squamates, Crocodilians and Rhynchocephalians. In: Biology of the Reptilia. C. Gans, D.W. Tinkle (Eds.) Academic Press, New York. 7: 157-264.

Dimaki et al. 2015

ACKNOWLEDGMENTS We wish to thank the people who helped in the fieldwork: Y. Ioannidis, Ph. Kokkini, Ch. Reppa, S. Roussos, and G. Maneas. Many thanks to "TEMES SA” for sponsoring the project in Peloponnese in 2013, NGO PELARGOS for the year 2014, and to E. Zimalis of the Museum of Natural History of Samos for the financial support during my field work on Samos island in 2000. Field work conducted under the following permits issued by the Ministry of Environment, Energy and Climate Change: No. 88794/4319 for 1997-1999, No. 201269/2731 for 2010-2011, No. 220834/2573 for 2011-2013, and No. 111541/1647 for 2014. Special thanks to Roger Butts for checking the language.

Short Note

Hyla

VOL. 2015., No.1, Str. 44 - 49 ISSN: 1848-2007

Đorđević & Anđelković 2015

Possible reproduction of the red-eared slider, Trachemys scripta elegans (Reptilia: Testudines: Emydidae), in Serbia, under natural conditions Moguća reprodukcija crvenouhe kornjače, Trachemys scripta elegans (Reptilia: Testudines: Emydidae), u Srbiji, u prirodnim uvjetima SONJA ĐORĐEVIĆ1,3, MARKO ANĐELKOVIĆ2 1

University of Belgrade, Faculty of Biology, Institute of Zoology, Studentski trg 16, 11000 Belgrade, Serbia, sonjadj@bio.bg.ac.rs 2 University of Belgrade, Institute for Biological Research “Siniša Stanković”, Despota Stefana Blvd. 142, 11000 Belgrade, Serbia 3 Serbian Herpetological Society “Milutin Radovanović”, Despota Stefana Blvd. 142, 11000 Belgrade, Serbia Abstract The North American chelonian, Trachemys scripta elegans, is still among the most popular pets worldwide. However, if released into natural water bodies outside of its natural distribution range it becomes a great nuisance and threat to native freshwater turtles and other aquatic wildlife. We report, for the first time, on the case of possible reproduction of the red-eared sliders under natural conditions in north-central Serbia. In July 2014 we found two red-eared slider hatchlings near the canal in the settlement of Borča near the Serbian capital. Judging by their body sizes and appearance (muddy shells, curved carapace), they had recently hatched near the place where they were found. Key words: Serbia, red-eared slider, reproduction

Sažetak Sjeverno-američka vrsta kornjače, Trachemys scripta elegans, danas je jedna od najpopularnijih kućnih ljubimaca širom Svijeta. Ipak, ako joj se omogući bijeg u prirodna staništa, postaje vrlo velik problem i prijetnja domaćoj barskoj kornjači i generalno vodenim životinjama. U ovom radu, po prvi put, izvještavamo o slučaju potencijalne reprodukcije crvenouhe kornjače u prirodnim uvijetima na području sjeverne i centralne Srbije. U srpnju 2014. Pronašli smo dva tek izlegla mladunca crvenouhe kornjače u blizini odvodnog kanala u selu Borča (okolica Beograda). Sudeći prema njihovoj duljini tijela i generalnim karakteristikama (blatni oklop, zabljeni karapaks), može se ustvrditi da su se tek izlegli vrlo blizo mjesta pronalaska. Ključne riječi: Srbija, crvenouha kornjača, reprodukcija Trachemys scripta (Schoepff, 1792) is an

2013). Trachemys species are popular pets, but they

aquatic turtle native to the New World (van Dijk et

are also used for human consumption or for

al. 2013); one of its three subspecies (Bringsøe

religious purposes (e.g. Ramsay et al. 2007, Mali et

2006), Trachemys scripta elegans (Wied-Neuwied,

al. 2014). For decades (between 1950’s and

1839), is listed among the 100 worst invasive alien

1970’s), app. 10 million individuals had been

species in the world (Scalera 2006; van Dijk et al.

imported annually into the Old World countries;

Short Note

Hyla

VOL. 2015., No.1, Str. 44 - 49 ISSN: 1848-2007

Đorđević & Anđelković 2015

during the 1980’s this rate lowered, but still, e.g. in

Import of T. s. elegans into the EU has been

1996, over 2 million individuals were imported into

banned since 1997 (Bringsøe 2006); however, other

Europe (Bringsøe 2006; Scalera 2006; Ramsay et

subspecies are being imported instead (van Dijk et

al. 2007). Between 1989 and 1997 a total of 52

al. 2013). Individual EU members also forbid the

million individuals were exported from the USA

trade in this species, but in some it can still be

farms (Cadi et al. 2004; Scalera 2006). Despite

easily bought, along with other allochthonous

legal restrictions, export rates of wild-caught and

chelonians (e.g. Kitowski & Pachol 2009, Semenov

commercially bred freshwater turtles from the USA

2010). In Serbia, T. scripta is listed as invasive

are still high (Mali et al. 2014). When these turtles

(Lazarević et al. 2012), and the import of all its

outgrow their aquaterraria, many owners decide to

subspecies is forbidden (Official Gazette of the

“release” their red-eared pets into natural or

Republic of Serbia No. 99/2009-26, 6/2014-9).

artificial water bodies; being highly resistant and

Nevertheless, it is still available for sale (Urošević

adaptable, they manage to survive and often to

et al. in press). On July 7th 2014, in the Belgrade

reproduce as well (Rödder et al 2009). Introduced populations of T. scripta

suburban settlement of Borča, along the Sebeš

already exist in numerous countries, on all

canal (44°52′14.60″N, 20°28′44.04″E, 69 m a.s.l),

continents except Antarctica (Cadi et al. 2004,

one of the authors (M. A.) found two hatchlings of

Ramsay et al. 2007, Pérez-Santigosa et al. 2008).

Trachemys scripta elegans. Borča lies on the left

The red-eared slider is often widely distributed in

bank of the Danube River. It belongs to the

its new territory (Cadi & Joly 2004; van Dijk et al.

biogeographic region of Banat, which is a part of

2013). In Europe, breeding populations of T.

the flat and moist lowlands of the Pannonian plain

scripta have also been documented, mostly in

(Marković 1970, Stevanović 1992). In this area

regions with a Mediterranean climate, where both

there is a natural wetland, and a huge pond further

sexes can be produced under natural incubation

from the river, but small artificial water bodies also

conditions (Cadi et al. 2004, Perez-Santigosa et al.

exist; several canals run through the settlement. In

2008, van Dijk et al. 2013). However, reproduction

these canals, M. A. observed Emys orbicularis (L.,

of T. scripta has already been recorded in several

1758) on several occasions.

localities with a more continental climate, e.g. in

One of the collected red-eared slider

Austria, Switzerland, Slovenia and, potentially, the

hatchlings was dead (probably run over by a

Czech Republic (Brejcha et al. 2009, Vamberger et

vehicle), but another was alive and healthy (Figure

al. 2012, van Dijk et al. 2013, Kleewein 2014).

1). The latter had straight carapace length of 28.3

The usual way of introducing these

mm, and its body weight was 4.6 g. This individual

animals outside of their natural range is a deliberate

was

release by their owners/breeders; therefore, they are

herpetological collection of the Faculty of Biology,

most abundant in urban and semi-urban habitats

University of Belgrade.

(Arvy & Servan 1996, 1998, Cadi et al. 2004, Bringsøe 2006, Semenov 2010, Dimancea 2013).

euthanized

and

will

kept

the

Tucker (2000) reported T. s. elegans hatchlings’ average carapace lengths of 31.6 mm

that

(the range he recorded was 27.0 mm – 35.4 mm);

“European populations are either tolerated or their

their average body mass was 6.92 g (3.94 g – 8.77

elimination is desired” (van Dijk et al. 2013).

g). Considering the size of the sliders we found, we

The

IUCN

authorities

decided

Short Note

Hyla

VOL. 2015., No.1, Str. 44 - 49 ISSN: 1848-2007

Đorđević & Anđelković 2015

presume that they could not have been released by

is strongly curved carapace of the live hatchling:

a negligent pet-owner, but probably hatched

Perez-Santigosa et al. (2008) noted that shells of

naturally, in the vicinity of one of the canals in

newly hatched sliders are highly domed.

Borča. Additional feature to support this possibility

Figure 1. Trachemys scripta elegans hatchlings found from Borča: A) the one found dead on the road; B) alive individual Slika 1. Netom izvaljeni mladunci vrste Trachemys scripta elegans iz Borča: A) jedinka pronađena mrtva na cesti; B) živa jedinka

Previously,

scripta

sufficient to enable T. scripta survival and

from

reproduction under natural conditions. Biology of

numerous places in Serbia (Džukić et al. 2008,

T. scripta elegans, its high potential for invasions

Lazarević et al. 2012, Urošević et al. in press). To

and interactions with native species have already

our knowledge, its reproduction in Serbia has not

been addressed by numerous researchers (Packard

previously been confirmed and publicised. It is

et al. 1997, Gist & Congdon 1998, Cadi & Joly

possible that the red-eared sliders breed in the

2003, 2004, Cadi et al. 2004, Bringsøe 2006,

public park in Novi Sad: a population of

Scalera 2006, Ultsch 2006, Perez-Santigosa et al.

approximately 150 individuals inhabits the park

2008, Polo-Cavia et al. 2008, 2011, 2012, Semenov

pond (Urošević et al. in press), and people reported

2010, van Dijk et al. 2013) and are out of the scope

seeing small turtles there. More importantly, we

of the present paper, hence we will not discuss

obtained reliable information from the veterinarian

them here.

specimens/populations

adult were

T. reported

in the Belgrade Zoo: T. elegans hatchlings were

On May 23rd 2015, at 12:45, photographs

found in the Zoo in 2013 and 2014 (the Zoo had

were made (Figure 2) of a large T. s. elegans

been accepting adult sliders, but no juveniles). In

female (carapace length about 25 cm) laying eggs

Serbia, moderate continental climate predominates.

in Novi Sad, on the sandy shore of a branch of

Тhe 2013/2014 winter was mild, and entire 2013

Danube between Kameničko ostrvo and the city

was extremely warm – seventh warmest in the past

(Sime

60 years (Republic Hydrometeorological Service of

19.821397E).

Matavulja

Street,

app.

45.231997N,

Serbia). Such climatic conditions apparently were 46

Short Note

Hyla

VOL. 2015., No.1, Str. 44 - 49 ISSN: 1848-2007

Đorđević & Anđelković 2015

Figure 2. A large red-eared slider laying eggs in Novi Sad (photo: Dejan Kolar) Slika 2. Velika crvenouha kornjača polaže jaja u Novom Sadu (fotografija: Dejan Kolar) The

possible

presence

breeding

med. vet. Özvegy József for reporting Trachemys

populations of a species with potentially significant

reproduction in the Belgrade Zoo. Dr Aleksandar

negative impacts on autochthonous fauna implies

Urošević hepled us improve the manuscript. Dejan

an emergent need to intensify the research

Kolar kindly allowed us to use and publicise his

concerning the ecology of native and invasive

finding and photograph of the nesting T. s. elegans

aquatic chelonians, and to strictly implement the

from Novi Sad. Two anonymous reviewers

existing legislation.

prevention of

provided helpful comments and recommendations.

introduction and spreading of invasive species is

Our work was partially financed by the grant

imperative. All subsequent investigation efforts,

173043 provided by the Ministry of Education,

control and eradication measures are time- and

Science and Technological Development of the

energy-consuming

Republic of Serbia.

A sound

and

extremely

expensive

(Scalera 2007, Valdeón et al. 2010), and their results and outcomes are uncertain.

Acknowledgements Some data on the presence of T. scripta elegans in Serbia were provided by people who contacted the Serbian Herpetological Society. We thank mr sci.

References Arvy, C. & Servan, J. (1996): Distribution of Trachemys scripta elegans in France: a potential competitor for Emys orbicularis. In Fritz, U., Joger, U., Podloucky, R., Servan, J. & Buskirk, J.R. (eds.) Proceedings of the EMYS Symposium, Dresden, Germany. Arvy, C. & Servan, J. (1998): Imminent competition between Trachemys scripta and 47

Hyla

VOL. 2015., No.1, Str. 44 - 49 ISSN: 1848-2007

Emys orbicularis in France. In Fritz, U. et al. (eds.) Proceedings of the EMYS Symposium Dresden 96. Mertensiella 10: 33–40. Brejcha, J., Miller, V., Jeřábková, L. & Šandera, M. (2009): Výskyt Trachemys scripta na území ČR [Distribution of pond slider (Trachemys scripta) in the Czech Republic]. Herpetologické Informace 8: 14–29. Bringsøe, H. (2006): NOBANIS – Invasive Alien Species Fact Sheet – Trachemysscripta. In Online Database of the North European and Baltic Network on Invasive Alien Species – NOBANIS, www.nobanis.org. Accessed on July 14, 2014. Cadi, A. & Joly, P. (2003): Competition for basking places between the endangered European pond turtle (Emys orbicularis galloitalica) and the introduced red-eared slider (Trachemys scripta elegans). Canadian Journal of Zoology 81: 1392–1398. Cadi, A. & Joly, P. (2004): Impact of the introduction of the red-eared slider (Trachemys scripta elegans) on survival rates of the European pond turtle (Emys orbicularis). Biodiversity and Conservation 13: 2511–2518. Cadi, A., Delmas, V., Prévot-Julliard, A.-C., Joly, P., Pieau, C. & Girondot, M. (2004): Successful reproduction of the introduced slider turtle (Trachemys scripta elegans) in the south of France. Aquatic Conservation: Marine and Freshwater Ecosystems 14: 237–246. Dimancea, N. (2013): Note upon the presence of Trachemys scripta elegans (Reptilia) in Oradea city, western Romania. Herpetologica Romanica 7: 41–47. Džukić, G., Kalezić, M. & Mesaroš, G. (2008): Barska kornjača (Emys orbicularis L.) u donjoj Panoniji: prošlost, sadašnjost, budućnost. Savetovanje: “Stanje i perspective populacija barske kornjače u Vojvodini”. pp. 1–29. In Proceedings of the Palić-Hajdukovo symposium “State and perspectives of the pond turtle populations i Vojvodina province”. Subotica, September 9th 2008. Gist, D. H. & Congdon, J. D. (1998): Oviductal sperm storage as a reproductive tactic of turtles. The Journal of Experimental Zoology 282: 526– 534. Kitowski, I. & Pachol, D. (2009): Monitoring the trade turnover of red-eared terrapins (Trachemys scripta elegans) in pet shops of the Lublin region, east Poland. North-Western Journal of Zoology 5: 34–39. Kleewein, A. (2014): Natural reproduction of Trachemys scripta troostii (Holbrook, 1836) x Trachemys scripta scripta (Schoepff, 1792) in Austria. Herpetozoa 26: 183–185. Lazarević, P., Stojanović, V., Jelić, I., Perić, R., Krsteski, B., Ajtić, R., Sekulić, N., Branković, S., Sekulić, G. & Bjedov, V. (2012): Preliminarni spisak invazivnih vrsta u Republici Srbiji sa

Short Note

Đorđević & Anđelković 2015

opštim merama kontrole i suzbijanja kao potpora budućim zakonskim aktima [Preliminary list of invasive species in the Republic of Serbia with general measures of control and management, as a background to future legal acts]. Protection of Nature 62: 5–32. Mali, I., Vandewege, M. W., Davis, S. K. & Forstner, M. R. J. (2014): Magnitude of the freshwater turtle exports from the US: long term trends and early effects of newly implemented harvest management regimes. PLoS ONE 9: e86478. Marković, J. Đ. (1970): Geografske oblasti Socijalističke Federativne Republike Jugoslavije [Geographical regions of the Socialist Federal Republic of Yugoslavia]. Zavod za udžbenike i nastavna sredstva Srbije, Beograd. Official Gazette of the Republic of Serbia 99/200926, 6/2014-9, Regulation on cross-border transport and trade of protected species: www.pravno-informacionisistem.rs/SlGlasnikPortal/pages/Package.xhtml#. Appendix VI, species referred to by the import prohibition of the paragraph 21 of the Regulation: www.pravno-informacionisistem.rs/SlGlasnikPortal/prilozi/prilog6.htm. Accessed on July 15, 2014. Packard, G. C., Tucker, J. K., Nicholson, D. & Packard, M. (1997): Cold tolerance in hatchling slider turtles (Trachemys scripta). Copeia 1997: 339–345. Pérez-Santigosa, N., Díaz-Paniagua, C. & HidalgoVila, J. (2008): The reproductive ecology of exotic Trachemys scripta elegans in an invaded area of southern Europe. Aquatic Conservation: Marine and Freshwater Ecosystems 18: 1302– 1310. Polo-Cavia N, López, P., & Martín, J. (2008): Interspecific differences in responses to predation risk may confer competitive advantages to invasive freshwater turtle species. Ethology 114: 115–123. Polo-Cavia, N., López, P. & Martín, J. (2011): Aggressive interactions during feeding between native and invasive freshwater turtles. Biological Invasions 13: 1387–1396. Polo-Cavia, N., López, P. & Martín, J. (2012): Feeding status and basking requirements of freshwater turtles in an invasion context. Physiology and Behavior 105: 1208–1213. Ramsay, N. F., Ng, P. K. A., O’Riordan, R. M. & Chou, L. M. (2007): The red-eared slider (Trachemys scripta elegans) in Asia: a review. pp. 161–174. In Gherardi, F. (eds.) Biological invaders in inland waters: profiles, distribution, and threats. Springer Publishing, The Netherlands. Republic Hydrometeorological Service of Serbia, Annual Bulletin for Serbia 2013. Available at

Hyla

VOL. 2015., No.1, Str. 44 - 49 ISSN: 1848-2007

www.hidmet.gov.rs/podaci/meteorologija/eng/20 13.pdf. Rödder, D., Schmidtlein, S., Veith M, & Lötters, S. (2009): Alien invasive slider turtle in unpredicted habitat: a matter of niche shift or of predictors studied? PLoS ONE 4: e7843. doi:10.1371/journal.pone.0007843. Scalera, R. (2006): Trachemys scripta. From: DAISIE (Delivering Alien Invasive Species Inventories for Europe), www.europe-aliens.org. Accessed on July 14, 2014. Scalera, R. (2007): Virtues and shortcomings of EU legal provisions for managing NIS: Rana catesbeiana and Trachemys scripta elegans as case studies. pp. 669–678. In Gherardi, F. (eds.) Biological invaders in inland waters: profiles, distribution, and threats. Springer Publishing, The Netherlands. Semenov, D. V. (2010): Slider turtle, Trachemys scripta elegans, as invasion threat (Reptilia; Testudines). Russian Journal of Biological Invasions 1: 296–300. Stevanović, V. (1992): Floristička podela teritorije Srbije sa pregledom viših horiona i odgovarajućih flornih elemenata. In: Sarić, M. R. (eds.): Flora Srbije 1: 47–56. Srpska akademija nauka i umetnosti, Beograd.

Short Note

Đorđević & Anđelković 2015

Tucker, J. K. (2000): Annual variation in hatchling size in the red-eared slider turtle (Trachemys scripta elegans). Herpetologica 56: 8–13. Ultsch, G. R. (2006): The ecology of overwintering among turtles: where turtles overwinter and its consequences. Biological Reviews 81: 339–367. Urošević, A., Tomović, L., Ajtić, R., Simović, A., Džukić, G. (in press): Alterations in the reptilian fauna of Serbia: introduction of exotic and anthropogenic range expansion of native species. Herpetozoa 28, scheduled for publishing in December 2015. Valdeón, A., Crespo-Diaz, A., Egaña-Callejo, A. & Gosá, A. (2010): Update of the pond slider Trachemys scripta (Schoepff, 1972) records in Navarre (northern Spain), and presentation of the Aranzadi turtle trap for its population control. Aquatic Invasions 5: 297–302. Vamberger, M., Lipovšek, G. & Gregorič, M. (2012): First reproduction record of Trachemys scripta (Schoepff, 1792), in Slovenia. Herpetozoa 25: 76–79. van Dijk, P. P., Harding, J. & Hammerson, G. A. (2013): Trachemys scripta. The IUCN Red List of Threatened Species. Version 2014.1. www.iucnredlist.org, www.iucnredlist.org/details/22028/0. Accessed on July 7, 2014.

Photo note

Hyla

VOL. 2015., No.1, Str. 50 - 52 ISSN: 1848-2007

Schweiger 2015

First record of breeding of the alien turtle species Trachemys scripta elegans in the wild on the island of Krk, Croatia? Prvi nalaz razmnožavanja strane invazivne vrste Trachemys scripta elegans u divljini na otoku Krku, Hrvatska? MARIO SCHWEIGER Vipersgarden, Katzelsberg 4, 5162 Obertrum, Ӧsterreich. E-mail: office@vipersgarden.at American turtles of different species have

No red-eared sliders have been sold, or hatchlings

been, or are still sold in pet shops. Most of these

imported into the EC since 1998, following the EC

species

directives EC 338/97 and EC 865/06.

grow,

especially

females,

large

dimensions, e.g. the red-eared slider to approx. 30

Vamberger, Lipovšek & Gregorić (2012) confirmed

cm carapace length. Therefore they are much too

the breeding of the species in south-western

large for keeping in most aquariums, for this reason

Slovenia.

many specimens are released into the wild across

The author therefore has the strong

Europe. On the Croatian island of Krk one may

assumption that this is the first record on breeding

encounter these turtles in many ponds. One of these

of this species for the island of Krk, maybe for the

is the Kimpi pond, northwest of the town of Krk.

whole of Croatia.

The author, together with different companions,

Jelić et al. (2014) had no data for reproduction of

visited this pond during most excursions to the

the species for anywhere in Croatia.

island between 2004 and 2015. Up to 2014, only

Effects on the local and native turtle Emys

red-eared sliders have been observed in the Kimpi

orbicularis are still fiercely debated. Competition

pond. During the 3 weeks of May, 2009 and 2014,

might be for basking sites, food, but also for nesting

courtship bevaviour (displaying males in front of

places. Jelić et al. (2014) suppose a negative effect

females) was observed, but no mating has been

on native Emys orbicularis by long term survey on

seen.

the red-eared terrapin, but give no detailed During the last fieldherping trip from May

information.

Schweiger

(2008a)

observed

14 to May 17 2015 Trachemys scripta scripta,

competition on basking sites between Trachemys

Trachemys s. elegans and Graptemys sp. (probably

scripta elegans and Emys orbicularis in three ponds

pseudogeographica) were seen.

on the island Krk, although there would have been

While most of the turtles have been adults, one

enough places to bask for all turtles. Cadi, A. &

hatchling from last year of Trachemys scripta

Joly, P. (1999) studied the competition between the

elegans has been spotted. Although no egg-laying

two species in experimental ponds, at basking sites,

or hatching could have been observed, the author

Trachemys scripta was the dominant species. On

strongly supports the hypothesis that the turtle

the other hand, the author (Schweiger, 2008b)

hatched from a nest, deposited by one of the female

observed and filmed Emys orbicularis together with

sliders, because it seems very unlikely, that a baby

Trachemys scripta elegans, basking together on a

slider had been released there.

floating tree trunk in a pond on the island without any visible competition regarding basking sites. 50

Hyla

VOL. 2015., No.1, Str. 50 - 52 ISSN: 1848-2007

Photo note Schweiger 2015

Figure 1. Kimpi pond (Photo: Mario Schweiger) Slika 1. Lokva Kimpi (Fotografija: Mario Schweiger)

Figure 2. Hatchling of Trachemys scripta elegans observed at Kimpi pond on Thursday, May 17th , 2015 (Photo: Gerhard Egretzberger) Slika 2. Tek izlegli mladunac Trachemys scripta elegans pronađen u lokvi Kimpi u četvrtak, 17.05.2015 (Fotografija: Gerhard Egretzberger) 51

Hyla

VOL. 2015., No.1, Str. 50 - 52 ISSN: 1848-2007

References Cadi, A. & Joly, P. (1999): The introduction of the slider turtle (Trachemys scripta elegans) in Europe: Competition for basking sites with the European pond turtle (Emys orbicularis). Chelonii 2: 95 - 97 Jelić, L., Janev Hutinec, B., Preradović, M., Jelić, D. (2014): Distribution and ecology of Trachemys scripta (Schoepff, 1792) in Croatia.- 1st Croatian symposium of invasive species. Book of Abstracts. Pp. 16 Schweiger, M. (2008): Faunenverfälschung an Hand mehrerer Beispiele von der kroatischen Insel Krk. ÖGH-Aktuell, 20: 14 – 16.

Photo note Schweiger 2015

Schweiger, M. (2008b): Emys orbicularis and Trachemys scripta elegans basking in pond on Krk island. YouTube movie: https://www.youtube.com/watch?v=6lpKImzQZx c Vamberger, M., Lipovšek, G. & Gregorić, M. (2012): First reproduction record of Trachemys scripta (SCHOEPFF, 1792), in Slovenia. Herpetozoa 25(1/2): 76 - 79

Original Scientific Paper Jelić & Jelić 2015

Hyla

VOL. 2015., No.1, Str. 53 - 64 ISSN: 1848-2007

Allochthonous species of Turtles in Croatia and Bosnia and Herzegovina Strane vrste kornjača u Hrvatskoj i Bosni i Hercegovini LANA JELIĆ1, DUŠAN JELIĆ2 1 2

Public institution Maksimir, Maksimirski perivoj 1, 10000 Zagreb, Croatia, lanamalovic@yahoo.com

Croatian Institute for Biodiversity, Croatian Herpetological Society HYLA, Lipovac I. br 7, 10000 Zagreb, Croatia

Abstract The release of reptiles imported for pet trade, by their owners, over decades has caused allochthonous species to become widespread in natural habitats all over the World. The turtles are among the most popular reptiles in the pet trade. There are reports of the presence of one allochthonous species of turtle (Trachemys scripta) on the Balkan Peninsula for the past 20-30 years. The presence of Pelodiscus sinensis, in Croatia was officially published in 2014 and the presence of Graptemys pseudogeographica kohnii has been known since 2006 but not scientifically published. We gathered data on distribution and presence of Trachemys scripta elegans, Trachemys scripta scripta, G. p. kohnii, G. p pseudogeographica. and P. sinensis and produced the distribution map which shows heterogeneity in terms of rural/urban territories. The single largest allochtonous population (mostly comprised of T. scripta) in Croatia is found in Maksimir park (city of Zagreb) numbering over 300 individuals. Key words: allochthonous, turtles, distribution, Croatia, Bosnia and Herzegovina

Sažetak Alohtone vrste gmazova postale su tijekom posljednjih godina normalna pojava u prirodnim staništima diljem Svijeta kao posljedice puštanja jedinki uzgojenih i uvezenih za trgovinu kućnim ljubimcima. Upravo kornjače su jedna od najpopularnijih grupa gmazova u trgovini kućnim ljubimcima. Prve pouzdane bilješke o uvozu i prisutnosti alohtonih vrsta kornjača (Trachemys scripta), na području Balkanskog poluotoka, potječu od prije 20 - 30 godina. Prvi nalazi o prisutnosti Pelodiscus sinensis, u Hrvatskoj, potječu iz 2014. godine a podatci o prisutnosti Graptemys pseudogeographica kohnii neslužbeno su poznati još od 2006. godine ali nisu bili objavljeni. Ovim radom okupili smo sve dostupne i nove podatke o rasprostranjenosti Trachemys scripta elegans, Trachemys scripta scripta, G. p. kohnii, G. p pseudogeographica. i P. sinensis, te izradili nove precizne karte distribucije. Podatci ukazuju na heterogenost nalaza u odnosu na ruralna/urbana područja. Največa pojedinačna populacija alohtonih kornjača (uglavnom sačinjena od T. scripta) u Hrvatskoj nalazi se u gradskom parku u Maksimiru (grad Zagreb) koja broji preko 300 jedinki. Ključne riječi: alohtone, kornjače, rasprostranjenost, Hrvatska, Bosna i Hercegovina INTRODUCTION Biological invasions have taken place since prehistoric times but today with a much

higher rate it has became a global issue and through mass

invasion

can

lead

global

species

homogenization (Ricciardi 2007, Kraus 2009). For 53

Original Scientific Paper Jelić & Jelić 2015

Hyla

VOL. 2015., No.1, Str. 53 - 64 ISSN: 1848-2007

years biologists have been pointing out that

Graptemys pseudogeographica (Gray, 1831) is also

biological

for

a species native to North American but with smaller

biodiversity, ecosystem services, the economy and

native range than Trachemys species (Ernst &

human health (Mooney & Hobbs 2000, Sandlund et

Lovich 2009). In its native range it is present with

al. 2001, Pejchar & Mooney 2009, Kopecký et al.

two subspecies: G. p. kohnii (Baur, 1890) and G. p.

2013). Not only that, invasive species can influence

pseudogeographica (Gray, 1831). As a pet animal it

the

and

is now among the most traded turtle species, with

intraspecific interactions, there are also examples of

annual export numbers very close to Trachemys

invasive species altering the evolutionary traits of

sspp. (European Commission 2013, Kopecký et al.

native species (Mooney & Hobbs 2000). The first

2013). For this reason it is now also present in some

step of biological invasion is the introduction of a

countries of the Europe (Spain, Austria, Italy)

species to a new environment (Shea & Chesson

(Egaña-Callejo 2007, Kleewein & Wöss 2009,

2002, Kraus 2009) so it is very important to have

Izquierdo et al. 2010, Kleewein & Wöss 2011,

data on allochthonous species in the natural habitat.

Kleewein 2014b, Ottonello et al. 2014).

The allochthonous reptiles through decades of pet

Pelodiscus sinensis (Wiegmann, 1834) in contrast

trade have become widespread in almost all parts of

to the previous mentioned species is native to Asia.

the World and in many types of habitats (Ficetola

It is very attractive for its beautiful and soft shell so

2008).

it has also been included in the pet trade and

invasion

native

fauna

through

serious

threat

interspecific

The turtles are among the most popular pet

become present in the wild in some countries of

reptiles in trade and Trachemys scripta (Schoepff,

Europe (Bosnia and Herzegovina – B&H, Croatia,

1792) is almost certainly the most popular species

Latvia, Slovenia) (Brejcha et al. 2013, Pupins &

among the turtles (Kraus 2009, Kopecky et al.

Pupina 2011).

2013).

The

pond

slider

turtles,

with

three

Three species of aquatic turtles are

subspecies, T. s. scripta (Schoepff, 1792), T. s.

registered in Croatia by the Checklist of Croatian

elegans (Wied-Neuwied, 1839) and T. s. troostii

amphibians and

(Holbrook, 1836), are native to south-eastern

orbicularis (Linnaeus 1758), Mauremys rivulata

United States but are captive bred around the World.

(Valenciennes, 1833) and the allochthonous T.

Through decades of a massive pet trade and

scripta. Trachemys is first recorded entering the

uncontrolled release in nature T. scripta has become

Balkan peninsula some 40 years ago (Džukić &

the most commonly introduced and therefore the

Kalezić 2004) and recently it was identified as a

most widespread turtle species in the World

threat for the native pond turtle, Emys orbicularis

(Ficetola et al. 2008, Ernst & Lovich 2009, Kraus

(Linnaeus, 1758), Janev Hutinec et al. 2006,

2009, Kopecký et al. 2013). As an alien species it is

Brejcha et al. 2013) Lončar (2006). Šalomon et al.

already present in 29 European countries (Ficetola

(2013) and Janev Hutinec & Kolačko (2013) also

et al. 2012). In some of them reproduction has also

mention T. scripta in Maksimir park (Zagreb,

been recorded but with variable success: Austria,

Croatia) in terms of E. orbicularis conservation

Italy, Spain, France and Slovenia (Luiselli et al.

activities. In Croatia the presence of Graptemys

1997, Martinez-Silvestre et al. 2001, Cadi et al.

species is known only since 2006 when one

2004, Pérez-Santigosa et al. 2008, Vamberger et al.

individual of G. p.kohnii was noted during

2012, Kleewein 2014a).

Trachemys monitoring (Lončar 2006 - photographic

reptiles (Jelić

2014): Emys

Original Scientific Paper JeliÄ&#x2021; & JeliÄ&#x2021; 2015

Hyla

VOL. 2015., No.1, Str. 53 - 64 ISSN: 1848-2007

evidence). This individual has been removed and

different reports, our own field surveys, and

since then this subspecies has not been recorded

colleagues with reliable knowledge. All data was

again. From the literature only one locality per

plotted as a UTM (10 Ă&#x2014; 10 km) grid in WGS 1984

country is known for the presence of P. sinensis, in

coordinate system as decimal degrees. Based on

Croatia (Maksimir; five records for the same

collected data the first distribution map of T. scripta,

location) and B&H (Mostarsko blato; one record)

G. pseudogeographica, P. sinensis and their

(Brejcha et al. 2013).

putative subspecies is given (Figure 1.). All unique

Our goal was to determine presence of all

Trachemys sp. locations (n=46) were attributed

allochthonous turtle species in Croatia and B&H

with data on the average distance to the nearest city

and to assemble the data on their distribution. In

with more than 10000 people. Measurements were

this study we present all available data on

made in ESRI ArcGis 9.3 based on Croatian

distribution of T. s. elegans, T. s. scripta, G. p.

administrative data (census from 2011). Distance

kohnii and P. sinensis and first records of

was measured from the record location to the city

introduction

centroid in kilometres (km). For our analysis we

and

distribution

pseudogeographica in Croatia.

consider localities closer than 15 kilometres away from city centroid as urban areas and all localities further away as rural. This separation is purely

MATERIAL AND METHODS In this paper we summarize all current distribution

records

collected

from

scientific

holistic and is only made for easier interpretation of the data. Statistical analysis was carried out in

publications, media resources on herpetofauna,

software PAST 2.06.

RESULTS

each locality. The most sightings of all alien turtles

In total, 100 records from 46 localities

(all mentioned species and subspecies) and the

were analysed, 94 records (40 localities) from

biggest population of T. scripta (>200 individuals)

Croatia and six (in six localities) from B&H. In

is reported from Zagreb city, Maksimir park, where

Croatia these localities covered 13 out of 20

five semi-artificial ponds (total area of 8,2 ha) were

counties and in B&H three out of 10 counties. In

built from 1839-1911.

both countries localities are distributed in all three

For T. scripta only in 16 % of the records

biogeographic regions (Continental, Alpine and

were more than 10 individuals observed, with a

Mediterranean). Only 18 % of the data originates

maximum of 242 individuals in the 3rd pond in

from literature records and 82 % correspond to new

Maksimir park (Zagreb). In 28 % between two and

observations. The most records were reported for T.

10 individuals were observed and in 56 % only one

scripta (86 records in 43 localities) (Table 1).

individual was observed. From 46 localities where

Graptemys species are represented only with five

T. scripta was recorded, 13 of them (28 %) were

records for five localities and Pelodiscus sinensis

located in rural areas and 33 (72 %) in urban areas

with nine records in six localities. Only Trachemys

(< 15 km from nearest city with >10000 people).

species were recorded with more than one

Exactly 50 % of these locations were located within

individual per locality. The maximum number of

5 km from the nearest city. A log linear model, of

individuals observed together is listed in Table 2 for

the distance to the nearest city and number of 55

Original Scientific Paper Jelić & Jelić 2015

Hyla

VOL. 2015., No.1, Str. 53 - 64 ISSN: 1848-2007

observed individuals per location, showed just

weak negative correlation (r= -0,2718; p= 0,0589).

Table 1. Number of recorded Trachemys scripta elegans and Trachemys scripta scripta in Croatia and Bosnia and Herzegovina in period 1999-2014. TRe (Total Records). UTM (number of UTM 10×10 km square with confirmed presence). NMax (Maximum number of individuals observed together). Mean (Mean number observed in a same locality). Total (Total turtles observed). Counties: Zagreb City (1), Zagreb County (2), Krapina-Zagorje County (3), Varaždin County (4), Brod-Posavina County (5), Bjelovar-Bilogora County (6), Osijek-Baranja County (7), Primorje-Gorski Kotar County (8), Lika-Senj county (9), Zadar County (10), Šibenik-Knin County (11), Split-Dalmatia County (12), Dubrovnik-Neretva County (13), Sarajevo CountyCanton (14), Hercegovina-Neretva County-Canton (15). Tablica 1. Ukupni broj zabilježenih jedinki Trachemys scripta elegans i Trachemys scripta scripta u Hrvatskoj i Bosni i Hercegovini u periodu 1999-2014. TRe (Ukupno nalaza). UTM (broj UTM 10×10 km polja sa potvrđenim prisustvom). NMax (maksimalan broj jedinki zabilježen na lokaciji). Mean (prosječan broj jedinki zabilježen na lokaciji). Total (broj ukupno viđenih jedinki). Županije: Zagrebačka (1), Zagreb (2), Krapinskozagorska (3), Varaždinska (4), Brodsko-posavska (5), Bjelovarsko-bilogorska (6), Osiječko-baranjska (7), Primorsko-goranska (8), Ličko-senjska (9), Zadarska (10), Šibensko-kninska (11), Splitsko-dalmatinska (12), Dubrovačko-neretvanska (13), Kanton Sarajevo (14), Hercegovačko-neretvanski kanton (15). Croatia

TRe UTM NMax Mean Total

(1) 44 4 242 20,5 900

(2) 3 2 1 1 3

(3) 2 2 21 11 22

(4) 1 1 2 2 2

(5) 1 1 2 2 2

(6) 2 2 2 1,5 3

(7) 1 1 1 1 1

(8) 20 7 2 1,2 23

(9) 1 1 1 1 1

(10) 1 1 2 2 2

(11) 3 2 38 16,3 49

(12) 2 2 6 3,5 7

(13) 1 1 1 1 1

Bosna and Herzegovina (14) (15) 3 1 3 1 30 1 13,7 1 41 1

Original Scientific Paper Jelić & Jelić 2015

Hyla

VOL. 2015., No.1, Str. 53 - 64 ISSN: 1848-2007

Table 2. Records of non-native turtle species in Croatia and Bosnia and Herzegovina during 1999-2014 (T.s. Trachemys scripta (unknown subspecies), T.s.s. - Trachemys scripta scripta, T.s.e - Trachemys scripta elegans, G.p. - Graptemys pseudogeographica (unknown subspecies), G.p.k. - Graptemys pseudogeographica kohnii, G.p.p. - Graptemys pseudogeographica pseudogeographica, G. sp. - Graptemys (unknown species), P.s. – Pelodiscus sinensis). Unpublished sources: ADNAN ZIMIĆ - (1), ANA ŠTIH - (2), BERISLAV HORVATIĆ - (3), BILJANA JANEV-HUTINEC - (4), DINA HLAVATI - (5), EDUARD KLETEČKI - (6), EMINA ŠUNJE - (7), IGOR VILAJ (8), IVAN BUDINSKI - (9), IVAN ŠPELIĆ - (10), IVO PERANIĆ - (11), KARMEN KARLUŠIĆ - (12), KREŠIMIR MIKULIĆ - (13), MARIO SCHWEIGER - (14), MARKO DOBOŠ - (15), MILA LONČAR - (16), MLADEN ZADRAVEC (17), PATRIK KRSTINIĆ - (18), PETAR VLCEK - (19), SENKA BAŠKIERA - (20), SLAVKO STRUNA - (21) and STJEPAN MEKINIĆ - (22). Tablica 2. Nalazi stranih vrsta kornjača u Hrvatskoj i Bosni i Hercegovini u razdoblju 1999-2014 (T.s. Trachemys scripta (nepoznata podvrsta), T.s.s. - Trachemys scripta scripta, T.s.e - Trachemys scripta elegans, G.p. - Graptemys pseudogeographica (nepoznata podvrsta), G.p.k. - Graptemys pseudogeographica kohnii, G.p.p. - Graptemys pseudogeographica pseudogeographica, G. sp. - Graptemys (nepoznata podvrsta), P.s. – Pelodiscus sinensis). Neobjavljeni izvori: ADNAN ZIMIĆ - (1), ANA ŠTIH - (2), BERISLAV HORVATIĆ - (3), BILJANA JANEV-HUTINEC - (4), DINA HLAVATI - (5), EDUARD KLETEČKI - (6), EMINA ŠUNJE - (7), IGOR VILAJ (8), IVAN BUDINSKI - (9), IVAN ŠPELIĆ - (10), IVO PERANIĆ - (11), KARMEN KARLUŠIĆ - (12), KREŠIMIR MIKULIĆ - (13), MARIO SCHWEIGER - (14), MARKO DOBOŠ - (15), MILA LONČAR - (16), MLADEN ZADRAVEC (17), PATRIK KRSTINIĆ - (18), PETAR VLCEK - (19), SENKA BAŠKIERA - (20), SLAVKO STRUNA - (21) i STJEPAN MEKINIĆ - (22). Geographic coordinates Locality

Lake in Bundek park (Zagreb) Lake in Botanical garden (Zagreb)

Jarun lake (Zagreb) Vrapčak stream (Špansko- Oranice, Zagreb) Vrapčak stream (Vukasova street) Kustošak stream (Trešnjevka, Zagreb)

First lake (Maksimir, Zagreb)

Year

T.s.e.

2014

Latitude, N 45,785267°

15,984014°

45,804906°

15,971572°

45,776496°

15,927268°

45,796790°

15,892369°

T.s.e.

16,098474° 15,931000°

45,891636° 45,794300°

45.9521666°

45,824037° 45,825266°

Notes and Pers.Com. (source)

UTM

28 specimens

WL77

14 specimens 7 specimens 13 specimens 6 specimens 1 specimen

WL77 WL77

2013

1specimen (2)

WL67

T.s.e.

2010

4 specimens (17)

WL77

T.s.e.

2012

1specimen (12)

WL77

P.s.

2010

T.s.e.

2012

T.s.s.

2013

T.s.e.

2012

16,021638°

T.s.s. G.p.p.

2013 2013

16,018595°

P.s.

2008

16.2884999 °

Second lake (Maksimir, Zagreb)

Third lake (Maksimir, Zagreb)

Species

Longitude, E

T.s.e. T.s.s. T.s.e. T.s.s. G.p.p.

2014

1 specimen (Brejcha et al. 2013) 43 specimens (4) 3 specimens (15) 23 specimens (4) 6 specimens 1 specimen 1 specimen (Brejcha et al.

WL76

WL77

Original Scientific Paper Jelić & Jelić 2015

Hyla

VOL. 2015., No.1, Str. 53 - 64 ISSN: 1848-2007

P.s.

2009

T.s.e. T.s.s. G.p.p.

2013

P.s.

2009

Fourth lake (Maksimir, Zagreb) T.s.e. 45,830487°

16,027507°

2013

T.s.s.

Fifth lake (Maksimir, Zagreb)

45,831955°

16,025499°

2013) 1 specimen (Brejcha et al. 2013) 242 specimens 10 specimens 2 specimens 1 specimen (Brejcha et al. 2013) 10 specimens (4) 1 specimen (15) 20 specimens (4) 1 specimen (15) 1 specimen (Lončar 2006)

WL77

T.s.e.

2012

T.s.s.

2013

G.p.k

2006

T.s.e.

2014

30 specimens

WL76

T.s.e.

2009

1 specimen (13)

WL77

T.s.e.

2011

1 specimen (11)

WL87

WL77 WL77 WL77

45,772382°

16,026906°

45,858422°

15,949171°

Sava River (Šćitarjevo)

45,778979°

16,138229°

Kupčina River (Kostanjevec)

45,697759°

15,473853°

T.s.e.

2011

1 specimen (21)

WL36

Finzula Lake (Rakitje)

45,800076°

15,828618 °

T.s.e.

2012

1 specimen (10)

WL67

45,794060°

15,840038°

T.s.e.

2012

1 specimen (10)

WL67

46,039522°

16,003593°

T.s.e.

2012

20 specimens (6)

WL79

46,140100°

15,880400°

T.s.e.

2013

1 specimen (2)

WM60

Trakošćan Lakes

46,260756°

15,937322°

T.s.e.

2013

2 specimens (8)

WM72

Sovsko lake (Dilj mountain)

45,287526°

18,014807°

T.s.e.

2009

BR61

Pond Bara (Grubišno polje)

45,664821°

17,149793°

45,599897° 45,494686°

17,226832° 18,095112°

2014

2 specimens (16) 2 specimens 1 specimen 1 specimen (20)

T.s.e.

2010

1 specimen (5)

BR74

Pond in city park on Sušak (Rijeka)

45,330546°

14,434855°

T.s.

2009

Pond on Pehlin (Rijeka) Podugrinac, well near house (Vinodol)

45,323738°

14,490792°

T.s.e.

45,152898°

14,769117°

45,034844°

14,558675°

45,054678°

14,649828°

Savica lakes (Zagreb) Kraljevac stream (Zagreb)

Nadolez Lake (Rakitje) Bedekovčanska Lakes (Hrvatsko Zagorje) On the road near Krapinjčica stream (Krapina)

Daruvar Našice, pond in city park

Kimpi pond on Krk Island Mišušalnica pond on Krk Island

T.s.e. P.s. T.s.s.

1999

XL65 YL05

2014

2 specimens (Š. D. 2009) 1specimen (18)

VL61

T.s.

2014

1specimen (16)

VK89

T.s.e.

2007

2 specimens (3)

VK68

T.s.e.

2009

2 specimens (3)

VK78

VL51

Original Scientific Paper Jelić & Jelić 2015

Hyla

VOL. 2015., No.1, Str. 53 - 64 ISSN: 1848-2007

Sv. Vid pond on Krk Island (Prniba)

45,015556°

14,621606°

T.s.e.

2 specimens (14)

VK78

Three ponds near Čižići on Krk Island

45,171103°

14,605842°

T.s.e.

Unknown (14)

VL60

45,080464°

14,555419°

T.s.e.

Unknown (14)

VK69

45,167489°

14,559089°

G.sp.

Unknown (14)

VL60

14.901563

T.s.e.

2007

1 specimen (Žagar et al. 2013)

VK93

T.s.e.

2002

2 specimens (6)

WK00

T.s.

2010

10 specimens

WJ74

T.s.e.

2013

1 specimen (9)

WJ75

T.s.

2006

1specimen (22)

XH69

6 specimens (22) 1specimen (19) 30 specimens (7)

XJ01

Ponikve lake on Krk Island Jezero lake on Krk Island Pag Island, Kolanjsko blato

44.558668

Vir Island, pond on Dočina

44,294035°

15,076168°

Šibenik, fountain in city park

43,734168°

15,894248°

43,815171°

15,925906°

43,250500°

17,089916°

Zbujača pond (Trogir)

43,525061°

16,239750°

T.s.e.

2011

Trsteno (Dalmacija)

42,715312°

17,977306°

T.s.

2007

Pionirska valey (Sarajevo, B&H)

43,878787°

18,413046°

T.s.e.

2012

Vrelo Bosne (near Igman mountain, B&H)

43,810178°

18,287651°

T.s.e.

2012

5 specimens (1)

BP85

Hutovo blato (Mostar, B&H)

43,062424°

17,785313°

T.s.e.

2013

1 specimen (HINA, 2013)

YH27

Garden pond in national museum in Sarajevo (B&H)

43,855090°

18,402655°

T.s.e.

2010

6 specimens

BP95

Rivina jaruga (Skradin) Staro selo (Podgora)

Mostarsko blato (B&H)

43,384346°

17,653113°

P.s.

2010

Bardača (B&H)

45,101463°

17,424284°

P.s.

2010

2 specimens (Brejcha et al. 2013) 1 specimen (Šikanjić 2010)

YH43 BP96

YJ10 BR82

Hyla

VOL. 2015., No.1, Str. 53 - 64 ISSN: 1848-2007

Original Scientific Paper JeliÄ&#x2021; & JeliÄ&#x2021; 2015

Figure 1. Distribution map with records of T. s. elegans, T. s. scripta, G. p. pseudogeographica, G. p. kohnii and P. sinensis in Croatia and B&H. Slika 1. Karta rasprostranjenosti sa nalazima T. s. elegans, T. s. scripta, G. p. pseudogeographica, G. p. kohnii i P. sinensis Hrvatskoj i Bosni i Hercegovini.

Original Scientific Paper Jelić & Jelić 2015

Hyla

VOL. 2015., No.1, Str. 53 - 64 ISSN: 1848-2007

especially in the city of Zagreb and its wider area. This is the direct result of the most intensive introduction of individuals, from pet trade, in this

Frequency

27 24

specific area (inhabited by around ¼ of Croatia’s

total population). In B&H still only individual

records are available, but this could be the result of

15 12

insufficient research. Although the occurrence of

reproduction of Trachemys is known from some

surrounding countries (Italy and Slovenia) (Luiselli

et al. 1997, Vamberger et al. 2012), we still suspect

0 0

that Croatian and B&H populations are mostly the

Kilometers from city (>10000 people)

Figure 2. Average distance of the Trachemys sp. location of sighting (n=46) to the nearest city center (only cities with more than 10000 people

consequence of individual pet owner’s releases. We assume that natural reproduction, if present, is probably very rare and egg and juvenile mortality is very high. Some juveniles manage to hatch and

were taken into account). Slika 2. Prosječna udaljenost nalazišta Trachemys sp. (n=46) do najbližeg gradskog centra (samo gradovi sa više od 10000 stanovnika su uzeti u

possibly survive to adulthood, but their numbers cannot be enough to maintain the population. The same was also indicated by Luiselli et al. 1997 for the Central Italian populations of T. scripta. We

obzir).

consider

maintained

DISCUSSION From three registered introduced species only T. scripta could be considered invasive. Records of G. pseudogeographica and P. sinensis are still just minimal. It is obvious that most of the Trachemys data corresponds to single individual observations and even though all individuals were not observed, these localities can be considered as localities without an established population. Some of the observed populations with more than 10 individuals are showing indications of stability over years and mostly even an increase in individual numbers. Reports of Trachemys introduction and naturalisation

that

are

available

from

countries

surrounding Croatia and B&H (Hungary, Italy, Slovenia, Serbia and Montenegro) (Puky et al. 2004, Ficetola et al. 2012, Lazarević et al. 2012, Žagar et al. 2013). From our data it is now justified to claim that Trachemys has become naturalised in Croatia,

our and

populations

are

primarily

increased

constant

anthropogenic input of new individuals from the pet trade. T. scripta occurs continuously over the whole region with most sightings in and close to urban areas (Figure 2.). This suggest a negative correlation between turtle density and distance from cities (as sources of introduction), but positive correlation between turtle density and concentration of human settlements. This is similar to data from other countries in their non native range (Arvy & Servan 1996). Few localities (Bundek lake, Jarun lakes, Savica lakes and Maksimir park) all in the urban area City of Zagreb, deserve our special attention in term of management actions because of the number of individuals and closeness or connection to a main river system (Sava River). All these localities are positioned upstream of nature protected areas Žutica, Turopolje and Lonjsko polje Nature Park, 61

Original Scientific Paper Jelić & Jelić 2015

Hyla

VOL. 2015., No.1, Str. 53 - 64 ISSN: 1848-2007

where large populations of E. orbicularis are present (Jelić et al. 2012). It is without question that these urban ponds act as invasion source and that animals can drift down into the natural habitats. Their fate there is unknown. These natural areas are usually very large and inaccessible for research therefore enabling the turtles to remain undetected. Bringsøe (2001) in term of successful invasion mentions that only small areas of southern Europe would have a suitable climate for slider turtles and Luiselli

al.

(1997)

suggested

limited

reproductive capability and a very low survival of juveniles, some authors however are predicting a possible increase in invasiveness due to recent climate change (Ficetola et al. 2008, Kikillus et al. 2010). Therefore this topic in our territory requires additional research based on up to date distribution data and predictive ecological models.

ACKNOWLEDGEMENTS We are grateful to ADNAN ZIMIĆ, ANA ŠTIH,

BERISLAV

HORVATIĆ,

BILJANA

JANEV

HUTINEC, BORIS LAUŠ, DAG TREER, DANIJEL JABLONSKI, DINA HLAVATI, DRAGICA ŠALOMON, EDUARD KLETEČKI, EMINA ŠUNJE, IGOR VILAJ, IVAN BUDINSKI, IVAN ŠPELIĆ, IVO PERANIĆ, JURICA STOŠIĆ, KARMEN KARLUŠIĆ, KREŠIMIR MIKULIĆ, MARIO SCHWEIGER, MARKO DOBOŠ, MILA LONČAR, MLADEN ZADRAVEC, PATRIK KRSTINIĆ, PETAR VLCEK, SENKA BAŠKIERA, SLAVKO STRUNA and STJEPAN MEKINIĆ for contributing with useful unpublished observations and photographs.

References Arvy, C. & Servan, J. (1996): Distribution of Trachemys scripta elegans in France: a potential competitor for Emys orbicularis. - In: Fritz, U., Joger, U., Podloucky, R., Servan, J. and Buskirk, J. R. (eds.), Proceedings of the EMYS Symposium. Dresden, Germany.

Brejcha, J., Cizelj, I., Marić, D., Vamberger, M. & Šanda, R. (2014): First records of the soft-shelled turtle, Pelodiscus sinensis (Wiegmann, 1834), in the Balkans. Herpetozoa 26 (3/4):189-192. Bringsøe, H. (2001): Trachemys scripta (Schoepff, 1792) – Buchstaben-Schmuckschildkröte’. In Fritz, U. (ed.) Handbuch der Reptilien und Amphibien Europas. Schildkröten (Testudines), AULA, Wiebelsheim. Cadi, A., Delmas, V., Prevot-Jullierd, A-C., Joly, P., Pieau, C. & Girodot, M. (2004): Successful reproduction of the introduced slider turtle (Trachemys scripta elegans) in the South of France. Aquatic Conservation: Marine and Freshwater Ecosystems 14: 237-246. Džukić, G. & Kalezić, M. (2004): The biodiversity of amphibians and reptiles in the Balkan Peninsula. In: Griffiths, H., Krystufek, B., Griffiths, J. (eds.): Balkan biodiversity. Papers from the ESF Exploratory Workshop on Balkan biodiversity - Koper, September 2001. Egaña-Callejo, A. (2007): Presencia y distribucion de los Galapagos exoticos en Gipuzkoa. Campaña 2007. Report, Aranzadi society of sciences, Herpetologia behatokia. European Commission (2013): Analysis of European Union and candidate countries annual reports to CITES 2011. UNEP-WCMC, Cambridge, <http://euanalysis2011.unepwcmc.org/species/graptemys-pseudogeographica4/>. Accessed on 14th October 2014. Ernst, C. H. & Lovich, E. J. (2009): Turtles of the United States and Canada, The Johns Hopkins University Press, Baltimor. Ficetola, G. F., Thuiller, W. & Padoa-Schioppa, E. (2008): From introduction to the establishment of alien species: a preliminary analysis of bioclimatic differences between presence and reproduction localities in Trachemys scripta. Herpetologia Sardiniae 8: 266-269. Ficetola, G. F., Rödder, D. & Padoa-Schioppa, E. (2012): Trachemys scripta (Slider terrapin). In Francis, R. A. (ed.) Handbook of global freshwater invasive species. Earthscan-Taylor & Francis Group, Abingdon. HINA (2013): Puštanje crvenouhe kornjače u Hutovo blato opasno po bioraznolikost Neretve i domaću kornjaču. Dnevno.hr [http://www.dnevno.hr/magazin/lifestyle/pustanje -crvenouhe-kornjace-u-hutovo-blato-opasno-pobioraznolikost-neretve-i-domacu-kornjacu100110]. Downloaded on 15.8.2015. Izquierdo, G. A., del Cueto, F. F., RodríguezPereira, A. & Avia, M.L. (2010): Distribution records of non-native terrapins in Castilla and León region (Central Spain) Aquatic Invasions 5(3): 303-308. 62

Hyla

VOL. 2015., No.1, Str. 53 - 64 ISSN: 1848-2007

Janev Hutinec, B., Kletečki, E., Lazar, B., Podnar Lešić, M., Skejić, J., Tadić, Z. & Tvrtković, N. (2006): Red book of amphibians and reptiles of Croatia. Ministry of Environmental and Nature protection, State Institute for Nature Protetction. Janev Hutinec B. & Kolačko G. (ed.) (2013): Priroda je (i) u gradovima. Agencija za zaštitu prirode i Javna ustanova “Maksimir”. Jelić D., Kuljerić, M., Koren, T., Treer, D., Šalamon, D., Lončar, M., Podnar Lešić, M., Janev Hutinec, B., Bogdanović, T., Mekinić, S. & Jelić, K. (2012): Red book of amphibians and reptiles of Croatia. Ministry of Environmental and Nature protection, State Institute for Nature Protetction. Jelić, D. (2014): Checklist of Croatian amphibians and reptiles with bibliography of 250 years of research. Natura Sloveniae 16(2): 17-72. Kikillus, K. H., Hare, K. M. & Hartley, S. (2010): Minimizing false-negatives when predicting the potential distribution of an invasive species: a bioclimatic envelope for the red-eared slider at global and regional scales. Animal Conservation 13(1): 5-15. Kleewein, A. & Wöss, G. (2009): Das Vorkommen von allochthonen Wasserschildkröten in Wien. Österreichische Gesellschaft für HerpetologieAktuell 22: 4-8. Kleewein, A. & Wöss, G. (2011): Zum Vorkommen von allochthonen Wasserschildkröten im Bundesland Salzburg. Mitteilungen aus dem Haus der Natur 19: 103-107. Kleewein, A. (2014a): Natural reproduction of Trachemys scripta troostii (Holbrook, 1836) x Trachemys scripta scripta (Schoepff, 1792) in Austria. Herpetozoa 26 (3/4):183-185. Kleewein, A. (2014b): Neue allochthone Wasserschildkrötenarten aus der Familie Emydidae in Kärnten, Carinthia II 204(124): 4146. Kopecký, O., Kalous, L. & Patoka, J. (2013): Establishment risk from pet-trade freshwater turtles in the European Union. Knowledge and Management of Aquatic Ecosystems 410(02):111. Kraus, F. (2009): Alien Reptiles and Amphibians: a Scientific Compendium and Analysis. Springer, New York. Lazarević, P., Stojanović, V., Jelić, I., Perić, R., Krsteski, B., Ajtić, R., Sekulić, N., Branković, S., Sekulić, G. & Bjedov, V. (2012): Preliminary list of invasive species in the Republic of Serbia with general measures of control and management, as a background to future legal acts. Protection of Nature 62(1): 5–32. Lončar, M. (2006): Monitoring of slider turtle (Trachemys scripta elegans) in Maksimir park, Report, Croatian Herpetological Society Hyla. Luiselli, L., Capula, M., Capizzi, D., Filippi, E., Jesus, V. T. & Anibaldi, C. (1997): Problems for

Original Scientific Paper Jelić & Jelić 2015

conservation of pond turtles (Emys orbicularis) in Central Italy: Is the introduced Red-Eared Turtle (Trachemys scripta) a serious threat? Chelonian Conservation and Biology 2: 417-419. Martinez-Silvestre, A., Soler-Massana, J., Sole, R. & Medina, D. (2001): Reproduccion de quelonios aloctonos en Cataluna en condiciones naturales. Boletín de la Asociación Herpetológica Española 12(1): 41-43. Mooney, H. A. & Hobbs, R. J. (eds.) (2000): Invasive Species in a Changing World. Island Press, Washington DC. Ottonello, D., Salvidio, S., Oneto, F., Jesu, R., Gili, C., Gnone, G., Lamagni, L., Ortale, S. & Genta, P. (2014): Conservation of Emys orbicularis in Liguria (NW Italy). Herpetological Facts Journal 1(1): 67-75. Pejchar, L. & Mooney, H. A. (2009): Invasive species, ecosystem services and human wellbeing. Trends in Ecology and Evolution 24(9):497-504. Pérez-Santigosa, N., Díaz-Paniagua, C. & HidalgoVila, J. (2008): The reproductive ecology of exotic Trachemys scripta elegans in an invaded area of southern Europe. Aquatic Conservation: Marine and Freshwater Ecosystems 18:1302-1310. Puky, M., Gémesi, D. & Schád, P. (2004): Distribution of Emys orbicularis in Hungary with notes on related conservational and environmental education activities. Biologia, Bratislava 59(14): 55-60. Pupins, M. & Pupina, A. (2011): First records of 5 allochthonous species and subspecies of Turtles (Trachemys scripta troostii, Mauremys caspica, Mauremys rivulata, Pelodiscus sinensis, Testudo horsfieldii) and new records of subspecies Trachemys scripta elegans in Latvia. Management of Biological Invasions 2:95-106. Ricciardi, A. (2007): Are modern biological invasions an unprecedented form of global change? Conservation Biology 21: 329-336. Sandlund, O. T., Schei, P. J. & Viken, A. (eds.) (2001): Invasive Species and Biodiversity Management. Kluwer Academic publishers, Dordrecht. Shea, K. & Chesson, P. (2002): Community ecology theory as a framework for biological invasions. Trends in Ecology & Evolution 17(4):170-176. Š. D. (2009): Kornjače u kanti za smeće, Rijeka danas, http://www.rijekadanas.com/kornjace-ukanti-za-smece/. Accessed on 20th October 2014. Šalamon, D., Janev Hutinec, B. & Lončar, M. (2013): Conservation activities for European pond turtles (Emys orbicularis) in Croatia. Herpetology Notes 6: 149-152. Šikanjić, T. (2010): Egzotične životinje ostavljaju u prirodi. Nezavisne novine, <http://www.nezavisne.com/novosti/drustvo/Egzo 63

Hyla

VOL. 2015., No.1, Str. 53 - 64 ISSN: 1848-2007

Original Scientific Paper Jelić & Jelić 2015

ticne-zivotinje-ostavljaju-u-prirodi-68969.html>. Accessed on 20th October 2014. Vamberger, M., Lipovek, G. & Gregori, M. (2012): First reproduction record of Trachemys scripta (Schoepff, 1792), in Slovenia. Herpetozoa 25 (1/2): 76-79. Žagar, A., Cafuta, V., Drašler, V., Jagar, T., Krofel, M., Lužnik, M., Ostanek, E., Petkovska, V., Planinc, G., Sopotnik, M. & Vamberger, M. (2013): A review of eleven short-term reptile surveys in the Western Balkans. Hyla 1: 3-21.

Short Note Stoyanov 2015

Hyla

VOL. 2015., No.1, Str. 65- 69 ISSN: 1848-2007

Registered high mortality of allochthon Red-eared Sliders (Trachemys scripta elegans) in an artificial pond in Sofia, Bulgaria

Registrirana visoka smrtnost alohtone crvenouhe kornjače (Trachemys scripta elegans) u umjetnom jezeru u Sofiji, Bugarska ANDREY STOYANOV National Museum of Natural History–Sofia, 1 Tsar Osvoboditel Blvd., 1000 Sofia, Bulgaria, astojanov12@gmail.com Abstract I report of finding six adult Red-eared sliders dead in an artificial pond in a park in Sofia, Bulgaria and stipulate on potential causes. I compare this case to similar occurrences in Bulgaria and elsewhere. Briefly, I discuss the potential issues from the presence of this non-native turtle, especially in small, isolated ponds. My aim is to draw attention of researchers to this unexplained mortality, encourage them to report similar observations and work towards finding the exact cause. Key words: Bulgaria, read-eared slider, high mortality

Sažetak U ovom radu prikazujem nalaz šest uginulih odraslih jedinki crvenouhe kornjače u umjetnom jezeru u gradskom parku u Sofiji, Bugarska, te diskutiram o potencijalnim uzrocima. Ovo opažanje uspoređeno je i sa drugim sličnim zabilježenim smrtnostima u Bugarskoj i drugdje. Ukratko diskutiram i druge potencijalne probleme uzrokovane širenjem ove strane invazivne vrste, posebice u malim izoliranim jezerima i lokvama. Cilj ovog rada je da se privuče pozornost drugih istraživača prema ovakvim neobjašnjenim povečanim smrtnostima , da ih se ohrabri da takve slučajeve objavljuju, te da multidisciplinarnim istraživanjima pokuša objasniti o čemu se točno radi. Ključne riječi: Bugarska, crvenouha kornjača, visoka stopa smrtnosti Information

for

aggregations

the

the problem or scientific publications were lacking.

allochthon species Red-eared slider Trachemys

Later, in two monographs the first published

scripta elegans in urban parks and park-like areas

scientific reports on the species appeared, describing

closely situated to cities have been previously

it as widely distributed in different water bodies

reported (e.g. by Philippen (1982), Kordges (1990),

throughout the whole country, with only a general

and Thiesmeier & Kordges (1990, 1991) for

map of the distribution was presented (besides a

Germany). By 2005, unpublished information on the

single location, the “Arboretum”) (Stojanov et al.

presence of this non-native species were obtained

2011; Tzankov et al. 2014). The most up to date

from most parts of Bulgaria, but an official study on

review for the country is presented by Tzankov et al. 65

Hyla

VOL. 2015., No.1, Str. 65- 69 ISSN: 1848-2007

Short Note Stoyanov 2015

(2015). In the beginning of May 2005, I visited one of

marsh was frozen, which probably led to shortage of

the major public parks in Sofia, Bulgaria, the South

oxygen in the water. The lack of a deeper layer of

Park. Within the park, a number of artificial

mud for the sliders to bury in and to avoid freezing

waterbodies (ponds) are situated, inhabited by native

also likely exacerbated the unfavorable conditions.

amphibians and reptiles: Marsh frog Pelophylax

My stipulation is supported by the fact that for the

ridibundus; Common toad Bufo bufo; Green toad

period November–March the mean air temperature

Bufotes viridis; Agile frog Rana dalmatina; Common

between 2000–2007 varied from 1.3–4.8°C, with

tree frog Hyla arborea; Southern (Balkan) crested

2005 experiencing one of the lowest, e.g. 1.6°C.

newt Triturus ivanbureschi; Smooth newt Lissotriton

Thus, I suppose that the individuals I found dead

vulgaris; Grass snake Natrix natrix; Dice snake N.

were released shortly prior to the beginning of the

tessellata and European pond turtle Emys orbicularis.

unfavorable weather condition and had no time to

Prior to 2005, within some of the water bodies a large

adapt and find suitable locations for overwintering.

number of individuals of the non-native Red-eared slider Trachemys scripta elegans were registered (author’s personal observations). During a survey of the first large pond in the central part of the South Park (N42.668160°; E23.307211°; Fig. 1) on May 1st 2005, on the shore and in the water I found dead six large, adult Redeared sliders (Fig. 2). The individuals had no visible external injuries, which speaks against the assumption of violent killing. I did not register dead E. orbicularis, a native species commonly observed there. I am not certain what killed them exactly

Figure 1. South park, Sofia – large, central pond, location of the dead Red-eared sliders (Photo: Axel Dehne).

because no additional tests were performed on the carcasses. The most probable explanation is the unusually cold weather during the previous winter

Slika 1. Južni park, Sofija – veliko, centralno jezero, mjesto pronalaska mrtvih crvenouhih kornjača (Slika: Axel Dehne).

months, when the majority of the water column of the

Short Note Stoyanov 2015

Hyla

VOL. 2015., No.1, Str. 65- 69 ISSN: 1848-2007

Figure 2. a) Dead adult Red-eared slider, Trachemys scripta elegans (Photo: Axel Dehne), b) Same dead individual – the solid bottom with limited amount of mud in the coastal, dry part of the pond (Photo: Axel Dehne). Slika 2. a) Uginula odrasla jedinka crvenouhe kornjače, Trachemys scripta elegans, (Slika: Axel Dehne), b) Ista uginula jedinka – kompaktno dno sa ograničenom količinom mulja u priobalnom, suhom djelu jezera (Slika: Axel Dehne). in a location are high enough. A confirmation, that Red-eared slider can endure very low temperatures during hibernation can be found by its continuous presence at an altitude of over 1,200 meters above sea level in the "Arboretum" at the nearby Vitosha Mountain (N42.627835°; E22.229138°), where its successful

overwintering

has

been

confirmed

(Stojanov et al. 2011; Tzankov et al. 2014). Similar information about high mortality during especially severe winters was provided by Bringsøe (2001): in 1964 in a shallow, forest pond in Jonstrup Vang, Figure 3. Live turtles, photographed on the same date at the same pond, that have presumably overwintered successfully (Photo: Axel Dehne). Slika 3. Žive kornjače, fotografirane na isti datum u istom jezeru, koje su uspješno preživjele hibernaciju (Slika: Axel Dehne).

Ballerup (near Copenhagen) 16 Red-eared slider were released; dead individuals were then found on the surface

during

the

first

winter,

but

because

individuals were observed in subsequent years, it is believed some survived. Bringsøe (2001) also states that sliders usually survive with minimal loses in waterbodies more than 2 m deep; similarly to my

Despite the presence of the dead individuals, I also recorded live specimens (Fig. 3), which

observations, he stipulates that the lack of oxygen is what likely causes such die-offs.

strongly suggests that the species is able to survive

No specific data exist on the actual number of

such extreme situations, especially when the numbers

released Red-eared sliders in the area of South Park, 67

Short Note Stoyanov 2015

Hyla

VOL. 2015., No.1, Str. 65- 69 ISSN: 1848-2007

but visual observations and expert evaluation suggest tens to hundreds of animals. This assumption is indirectly supported by the fact that the park facility and the discussed pond are located within the capital city of Sofia and human attendance for recreation there is very high. The proximity, the size of the water areas and the easy access suggest that this location will be preferred as an opportunity for the release of unwanted turtles compared to other alternatives outside the city (likely associated with elevated transport costs and invested time). Another understandable mistake of "nature lovers" is their association of habitats within a city park with wild nature, which is the natural environment of the home

Figure 4. Pike (Esox lucius), suffocated at the shore of Choklyovo swamp, 2012. (Photo: Andrey Stoyanov).

grown, exotic species. I observed a similar die-off in the spring of 2012 in a much larger body of water – the Choklyovo

Slika 4. Štuka (Esox lucius), uginula od gušenja u močvari Choklyovo 2012. godine (Slika: Andrey Stoyanov)

swamp (N42.398094°, E22.825982°), with a mass extinction of fish after extremely cold winters and deep freezing of the water column in the basin (Fig. 4). Such incidents with fish have been previously reported, including in relation to Red-eared sliders (Bringsøe 2001).

Usually the main negative impact of the invasive T. s. elegans that is discussed is mostly related to its role as a direct competitor for resources to the indigenous species of aquatic turtles (habitat, feeding grounds, etc.). However, observations in

The waterbody is inhabited by E. orbicularis

Germany demonstrate that the Red-eared slider feeds

as well; I found no dead turtles. The better conditions

on species such as the Marsh frog (P. ridibundus) and

for overwintering for turtles (e.g. larger area and

various species of newt (Klewen 1988, Klewen &

depth of the lake, as well as deeper layers of silt) are

Müller 1988). A justified assumption is that possible

probable conditions that had allowed the European

victims can be the juveniles of the two native species

pond turtles observed there to overcome (supposedly

of water snakes, based on findings of predation of

without losses) the adverse climatic conditions of the

juvenile animal of the genus Nerodia in North

particular year.

America (Goodman & Stewart 1998). These concerns should significantly expand the potentially harmful influence of this non-native predator on the local herpetofauna and biodiversity. This should be considered especially for small, isolated waterbodies, as is the

present case.

In addition,

serious 68

Short Note Stoyanov 2015

Hyla

VOL. 2015., No.1, Str. 65- 69 ISSN: 1848-2007

consideration

deserve

individual

messages

for

possible cases of successful breeding in more northern latitudes than Bulgaria (Gemel et al. 2005; Pieh & Laufer 2006), which suggest that future issues with this species will exacerbate. Due to difficulties with the artificial removal from the wild of the Redeared slider, natural limiting factors such as extremely cold weather might be an important, auxiliary means for limiting their distribution in non-native habitats.

Acknowledgements: I thank Axel Dehne for providing the photographs. Yurii Kornilev and an anonymous reviewer improved the manuscript.

References: Bringsøe, H. (2001): Trachemys scripta (Schoepff, 1792) – Buchstaben-Schmuckschildkröte:. In: Fritz, U. (Hrsg.), Handbuch der Reptilien und Amphibien Europas, Band 3/IIIA: Schildkröten (Testudines) I: 525–583. Wiebelsheim (Aula). Gemel, R., M. Marolt & G. Ochsenhofer (2005): Ungewöhnliche »Naturbrut« einer RotwangenSchmuckschildkröte (Trachemys scripta elegans) in der Südsteiermark. ÖGH-Aktuell 15: 9–11. Goodman, R. H. & G. R. Stewart (1998): Natural history notes: Testudines, Clemmys marmorata pallida (Southwestern pond turtle): coprophagy. Herpetological Review 29: 98. Klewen, R. (1988): Verbreitung und Ökologie der Wasserfrösche in Nordrhein-Westfalen und ihre Bestandssituation im Ballungsraum Duisburg/Oberhausen. Jahrbuch für Feldherpetologie, Beiheft 1: 73–96. Klewen, R. & A. Müller (1988): Aspekte des Artenund Naturschutzes. Abhandlungen aus dem Westfälischen Museum für Naturkunde Münster 50: 102–115. Kordges, T. (1990): Faunenverfälschung im Ballungsraum, dargestellt am Beispiel nordamerikanischer RotwangenSchmuckschildkröten (Chrysemys scripta elegans). NZ NRW Seminarberichte Recklinghausen 9: 36– 41. Philippen, H.-D. (1982): Freilebende Population von Chrysemys scripta elegans. Die Schildkröte 4/1–2: 24–34. Pieh, A. & H. Laufer (2006): Die RotwangenSchmuckschildkröte (Trachemys scripta elegans) in

Baden-Württemberg – mit Hinweis auf eine Reproduktion im Freiland. Zeitschrift für Feldherpetologie 13: 225–234. Stojanov, A. N. Tzankov, B. Naumov (2011): Die Amphibien und Reptilien Bulgariens. Edition Chimaira – Frankfurt am Main, s. 592. Thiesmeier, B. & T. Kordges (1990): Versuch einer ökologischen Klassifizierung der Amphibien- und Reptilienfauna des mittleren und östlichen Ruhrgebietes. Decheniana 143: 222–231. Thiesmeier, B. & T. Kordges (1991): Leitlinien zur ökologischen Verbesserung städtischer Teiche in Parkund Grünanlagen unter besonderer Berücksichtigung der Amphibienfauna. In: Schuhmacher, H. & B. Thiesmeier (Hrsg.): Urbane Gewässer: 103–113. Essen (Westarp). Tzankov, N. D., G. S. Popgeorgiev, B. Y. Naumov, A. Y. Stoyanov, Y. V. Kornilev, B. P. Petrov, A. V. Dyugmedzhiev, V. S. Vergilov, R. D. Draganova, S. P. Lukanov, A. E. Westerström. (2014). Identification guide of the amphibians and reptiles in Vitosha Nature Park. Directorate of Vitosha Nature Park, Sofia, p. 248. Tzankov, N., G. Popgeorgiev, Y. Kornilev, N. Natchev, A. Stoyanov, B. Naumov, I. Ivanchev (2015). First survey on the invasive Pond slider (Trachemys scripta) in Bulgaria: historic development and current situation. HYLA 2015(1): 18–27.

Short Note Grano & Cattaneo 2015

Hyla

VOL. 2015., No.1, Str. 70- 75 ISSN: 1848-2007

A survey on the presence of the invasive alien American bullfrog, Lithobates catesbeianus (Shaw, 1802) (Amphibia Anura Ranidae) in Latium (Central Italy) with reference to a possible infection of Batrachochytrium dendrobatidis on Bufo bufo Istraživanje prisustva invazivne Američke zelene žabe, Lithobates catesbeianus (Shaw, 1802) (Amphibia Anura Ranidae) u Latiumu (Centralna Italija) sa osvrtom na potencijalnu zarazu jedinke Bufo bufo sa gljivicom Batrachochytrium dendrobatidis MAURO GRANO¹ & CRISTINA CATTANEO²

Via Valcenischia 24, 00141Roma, Italy; e-mail: elaphe58@yahoo.it ² Via Eleonora d’Arborea 12, 00162 Roma, Italy; e-mail: cristina.cattaneo76@libero.it

Abstract The aim of this paper is to analyze the presence of the American bullfrog in Latium and its expansion in recent years. In this regard are given two unpublished reports. We want to pay specific attention on the discovery of a specimen of Bufo bufo probably affected by Batrachochytrium dendrobatidis. Key words: American bullfrog, Invasive alien species, Lithobates catesbeianus, Latium, Italy

Sažetak Cilj ovog istraživanja jest analiza prisustva Američke zelene žabe na području Latiuma, te njezino širenje tijekom posljednjih par godina. U skladu s tim ovdije prezentiramo dva nova nalaza ove vrste. Želja nam je posvetiti posebnu pozornost na zabilješku jedinke Bufo bufo vrlo vjerojatno zaraženu Batrachochytrium dendrobatidis. Ključne riječi: Invazivne strane vrste, Lithobates catesbeianus, Latium, Italija

Lithobates catesbeianus Shaw, 1802 is an

Witmer 2010). Furthermore, the American bullfrog is

amphibian of family Ranidae, native to North America.

known to act as a vector for Batrachochytrium

It is a big frog since it is able to exceed 30 cm in length

dendrobatidis dispersion (Hanselmann et al. 2004,

and 1600 g of weight (Lanza 1983). The females are

Garner et al. 2006, Federici et al. 2008, Dejean et al.

larger than the males. A very large and obvious

2010, Ficetola & Scali 2010). This fungus is largely

tympanic membrane is present in the temporal area.

implicated in global amphibian’s declines (Berger et al.

Bullfrog changes in color, above from dark olive to

1998, Blaustein & Kiesecker 2002, Mazzoni et al.

pale green, beneath from white to cream. This anuran is

2003, Kats & Ferrer 2003).

not only an efficacious competitor to native species but

The American bullfrog is listed on the list of

it is, also, an omnivore that feeds on all animals smaller

“100 of the world’s worst invasive alien species”.

than itself, including fishes, reptiles, amphibians and

These species were selected using two criteria: their

water birds (Lambertz & Schmied 2010, Snow &

serious impact on biological diversity and/or human 70

Short Note Grano & Cattaneo 2015

Hyla

VOL. 2015., No.1, Str. 70- 75 ISSN: 1848-2007

activities, and their illustration of important issues of

For drafting of this paper has been consulted

biological invasion (Lowe et al. 2000). In Italy this

the bibliography regarding the American bullfrog in

species is under CITES regulation (All. B, Directive

Europe and in Italy. The authors have conducted field

works and they availed themselves of unpublished data

101/2012)

(G.U.U.E.

2012),

because

its

introduction represents a threat to indigenous species (Di Cerbo & Biancardi 2013).

of some colleagues. The oldest report of Lithobates catesbeianus

In Europe its presence is confirmed, as well as

in Latium refers to 1969 at Pomezia in the province of

for Italy, also for Belgium (Wallonia, Flanders), France

Rome (Bruno 1969).

(Bordeaux), Germany (Bonn, Baden-Wurttemberg),

In the Atlas of Amphibians and Reptiles of Latium of

United

(Crete),

2000, the American bullfrog is reported only in three

Netherlands, (Breda) and Spain (Canary Islands,

localities: Maccarese - Torre in Pietra (Zona 40),

Cáceres, Cataluña). It’s possible that the population of

Pomezia (Rio Torto) and Tor San Lorenzo (Colle

United Kingdom has currently been eradicated. It was

Romito). The specimens imported in Maccarese in

probably introduced to Switzerland, although this

1974, came from Castel d’Ario (MN), the origin place

requires further confirmation (Santos-Barrera et al.

of the owner of the three sport fishing lakes in this

2009). In Italy the introduction of Lithobates

locality. In the same Atlas is mentioned that already in

catesbeianus, through specimens from Louisiana

1996 the Maccarese populations was missing, possibly

(U.S.A.), is dated to the thirties of last century and

due to the restructuring of the lakes where the

seems to be related to food purposes (Albertini &

American bullfrog was present (Bagnoli 2000). In the

Lanza 1988, Capula et al. 2005). The first successfully

following Atlas of Amphibians and Reptiles of

acclimatization occurred between 1932 and 1937 in the

Province of Rome of 2007, the earlier reports were

Corte Brusca district (Bigarello, Mantova) through

confirmed, bringing however into question their current

frogs released by Mr. G. Cavallero (Albertini 1970),

presence (Bologna et al. 2000), although some reports

and it would spread in short time in other territories by

confirm its presence in Maccarese. These reports are

some farmers who would use it for edible purposes

related to vocalizations heard in July 2005 in the area

(Albertini & Lanza 1988). In few years the Bullfrog

of “Vasche di Maccarese” and to sightings of

expanded itself to the point that, at the end of the

specimens in adjacent canals to Via delle Pagliete, Via

eighties the species was known in more than 160 sites

dei Collettori, Via dei Tre Denari and in the small pond

(Scali 2010). Currently the presence of Bullfrog in Italy

of plant nursery of the Maccarese Spa (Bologna, Rome,

is less considerable, but there are reports for Lombardy

pers. comm. 2014). A recent paper has confirmed the

(Bergamo, Brescia, Cremona and Pavia), Veneto

presence of L. catesbeianus in the canals of Viale

(Verona and Rovigo), Piedmont (Asti and Torino),

Maria at Maccarese (Pizzuti Piccoli & Cattaneo 2008).

Emilia-Romagna (Bologna, Modena, Ferrara, Piacenza

Through the years the transformation of the crops and

and Reggio Emilia), Tuscany (Firenze, Pisa and

irrigation techniques has been modified and it has had a

Pistoia) and Latium (Latina and in province of Rome:

decisive influence on the decline of populations of the

Maccarese, Torre in Pietra, Pomezia, Tor San Lorenzo,

whole Maccarese area. In November 2014, a spill of

Monterotondo Scalo, Fiano Romano and Civitella San

kerosene used as a fuel in the near International Airport

Paolo, Trigoria). Specimens were introduced in the

of Fiumicino, created a huge environmental catastrophe

provinces of Vercelli, Novara and Udine but without

in the whole area between Maccarese and Palidoro.

acclimatization (Lanza et. al. 2007).

Over 30 tons of kerosene has contaminated Rio Tre

Kingdom

(Surrey),

Greece

Short Note Grano & Cattaneo 2015

Hyla

VOL. 2015., No.1, Str. 70- 75 ISSN: 1848-2007

Cannelle and tens of surrounding hectares, killing

Strada Statale 156 of Monti Lepini at Latina. In these

thousands of fishes, frogs, turtles, shrimps and water

lakes there are many tadpoles and adults of American

birds. This serious episode allowed to verify that

bullfrog (Carlino, Rome, pers. comm. 2015).

among the thousands of dead animals was not present

Unfortunately a specimen of common toad Bufo bufo

any American bullfrog (Di Giuseppe, Maccarese, pers.

with severe skin lesions (Fig. 3), perhaps referable to

comm. 2014; Polinori, Ostia, pers. comm. 2014).

Batrachochytrium dendrobatidis, has been retrieved

Therefore, we can state that in the area of Maccarese,

from “Centro Recupero Fauna Selvatica, Lipu” of

Lithobates catesbeianus can be considered absent.

Rome (Manzia, Rome, pers. comm. 2014). Fragments

In 2014 a very large population of American bullfrog

tissue were promptly collected and sent to a specialized

(Fig.1) has been reported in a group of four small lakes

laboratory in order to confirm the diagnosis; we are

in locality Semblera, Monterotondo Scalo, along Via

currently waiting for a response. If the result of these

Salaria about twenty kilometers from Rome. This area

analyzes will be positive, it would be a serious problem

is adjacent to the left bank of Tevere River. Originally

for indigenous amphibians populations.

these small lakes were clay quarries used by a brick factory. At the end of the eighties these quarries were abandoned,

filled

with

waste

materials

and

subsequently with water. Initially, one of these ponds was used for sport fishing. Later they were no longer used and this allowed the rooting of luxuriant vegetation (Grano & Cattaneo 2014). In the same paper, the authors indicate another report of American bullfrog in province of Rome. This report refers to some quarries currently filled with water, located between Fiano Romano and Civitella San Paolo. Furthermore these quarries are placed nearby the Tevere River and are about twenty kilometers from the other quarries of Monterotondo Scalo (Grano &

Figure 1. Specimens of American Bullfrog found in a lake of Monterotondo Scalo (Rome). Slika 1. Jedinka Američke zelene žabe pronađene u jezeru Monterotondo Scalo (Rim).

Cattaneo 2014). For the first time we report the presence of Lithobates catesbeianus in the area of Trigoria, a fraction of Rome of the twelfth kilometer of Via Laurentina.

The

specimens

were

found

ornamental pond of a residential center. The big tadpole (Fig. 2) were photographed and sent to “Centro Recupero di Fauna Selvatica, Lipu” at Rome for the determination (Manzia, Rome, pers. comm. 2014). The most recent report, never reported before, regards the only locality of Latium that it’s not in the province of Rome. It’s a group of lakes utilized for sport fishing and for the rearing of ornamental fish, located on the

Figure 2. Big tadpole of American Bullfrog photographed in a pond of Trigoria (Rome). Slika 2. Punoglavac Američke zelene žabe fotografiran u jezeru u Trigoriji (Rim). 72

Short Note Grano & Cattaneo 2015

Hyla

VOL. 2015., No.1, Str. 70- 75 ISSN: 1848-2007

Acknowledgments We are grateful to Augusto Cattaneo for his invaluable help. We are also thankful to Marco A. Bologna Riccardo

(Università di

degli

Giuseppe

Studi (WWF

“Roma –

Tre”),

Oasi

Macchiagrande), Alessandro Polinori (Lipu – Oasi CHM di Ostia), Francesca Manzia (Lipu – Centro Recupero Fauna Selvatica, Roma) and Davide Carlino.

REFERENCES Figure 3. Bufo bufo affected by several skin lesions. Albertini, G. (1970): Sulla diffusione della rana-toro (Rana catesbeiana Shaw) importata nel Mantovano. Atti Memorie Accad. Agric. Sci. Lett. Verona (6) 20: 67-106.

Slika 3. Bufo bufo sa izraženim lezijama na koži

In Latium, the American bullfrog is regularly present from over forty years and during the last year has been reported four new localities. Recent studies (Ficetola et al. 2008) have shown that the Italian populations of L. catesbeianus have originated from a considerably small strain (less than six females), thus highlighting the great expansion capacity and rooting of this invasive frog (Scali 2010). Therefore, it is necessary to carry out regular

Albertini, G., Lanza, B. (1988): Rana catesbeiana Shaw, 1802 in Italy. Alytes 6 (3-4): 117-129. Andreone, F. (2005): Rane rosse e rane verdi: dilemmi fra tassonomia, sistematica zoologica e conservazione pp. 9-18. In: Le rane in risaia. Tradizione, scienza e risorsa. Convegno nazionale. Atti e interventi. Andreone, F., Marocco, R. (1999): Rana catesbeiana (Shaw, 1802) pp. 192-193. In Andreone, F. & Sindaco, R. (eds): Erpetologia del Piemonte e della Valle d’Aosta. Atlante degli Anfibi e dei Rettili, Monografie XXVI (1998), Museo Regionale di Scienze Naturali, Torino.

monitoring activities in order to record in time and to avoid eventual invasive processes, especially in the colonization of other new sites also due the strong impact which may exert on ecology and community structure of endemic amphibians (Andreone

Marocco 1999, Bologna et al. 2000). Furthermore the introduction of fish for sport fishing should be monitored with particular attention. It’s common practice, at least in Italy, populate the sport fishing lakes with a mixture of juvenile fishes coming from areas close to Mantova, where L. catesbeianus is certainly present whit large populations, therefore, together with the juvenile fishes may have been many tadpoles of American bullfrog (Andreone 2005, Ferri 2006).

Bagnoli, C. (2000): Rana catesbeiana (Shaw, 1802) pp. 66-67. In Bologna, M.A., Capula, M., Carpaneto, G.M. (eds.): Anfibi e Rettili del Lazio. Fratelli Palombi Editori, Roma. Blaustein, A.R., Kiesecker, J.M. (2002): Complexity in conservation: lessons from the global decline of amphibian populations. Ecology Letters 5: 597-608. Berger, L., Speare, R., Daszak, P., Green, D.E., Cunnigham, A.A., Goggin, G.L., Slocombe, R., Ragan, M.A., Hyatt, A.D., Mc Donald, K.R., Hines, H.B., Lips, K.R., Marantelli, G., Parkes, H. (1998): Chytridiomicosis causes amphibians mortality associated with population declines in the rain forest of Australia and Central America. Proc. Natl. Acad. Sci. Unit. States Am. 5: 9031-9036. Bologna, M.A., Capula, M., Carpaneto, G.M. (eds.) (2000): Anfibi e Rettili del Lazio. Fratelli Palombi Editori, Roma.

Hyla

VOL. 2015., No.1, Str. 70- 75 ISSN: 1848-2007

Bruno, S. (1969): Anfibi. In: Enciclopedia Italiana delle Scienze Naturali. Gli animali vertebrati, 1. Istituto Geografico D’Agostini, Novara. Capula, M., Ceccarelli, A., Luiselli, L. (2005): Amphibians of Italy: A revised checklist. Aldrovandia 1 (2005): 103-110. Dejean, T., Miaud, C. & Ouellet, M. (2010): La chytridiomycose: une maladie émergente des amphibiens. Bull. Soc. Herp. Fr. 134: 27-46. Di Cerbo, A.R., Biancardi, C.M. (2013): Ecological notes on the Bullfrog Lithobates catesbeianus in an area of the Po plain (Emilia-Romagna, Northern Italy). In Scillitani, G., Liuzzi, C., Lorusso, L., Mastropasqua, F., Ventrella, P.: Atti del IX Congresso Nazionale della Societas Herpetologica Italica (Bari-Conversano, 26-30 Settembre 2012). Pineta, Conversano. Federici, S., Clemenzi, S., Favelli, M., Tessa, G., Andreone, F., Casiraghi, M., Crottini, A. (2008): Identification of the pathogen Batrachochytrium dendrobatidis in amphibian populations of a plain area in the Northwest of Italy. Herpetology Notes 1: 033-037. Ferri, V. (2006): Rana catesbeiana Shaw, 1802, pp. 330-333. In Sindaco, R., Doria, G., Razzetti, E. & Bernini, F.: Atlante degli Anfibi e dei Rettili d’Italia. Edizioni Polistampa, Firenze. Ficetola, G.F., Bonin, L. & Miaud, C. (2008): Population genetics reveals origin and number of founders in a biological invasion. Molecular Ecology 17: 773-782. Ficetola, G.F., Scali, S. (2010): Invasive Amphibians and Reptiles in Italy. In Di Tizio, L., Di Cerbo, A.R., Di Francesco, N., Cameli, A. (eds.): Atti. VIII Congresso Nazionale Societas Herpetologica Italica (Chieti, 22-26 Settembre 2010), Ianieri Edizioni, Pescara. Garner, T.W.J., Perkins, M.W., Govindarajulu, P., Seglie, D., Malker, S., Cunnigham, A.A., Fischer, M.C. (2006): The emerging amphibian pathogen Batrachochytrium dendrobatidis globally infects introduced populations of the North American bullfrog, Rana catesbeiana. Biology Letters 2: 455459. Gazzetta Ufficiale dell’Unione Europea (G.U.U.E.), (2012): Regolamento (UE) n. 101/2012, L 39: 133200. Grano, M., Cattaneo, C. (2014): A new record for the American Bullfrog, Lithobates catesbeianus (Shaw, 1802) (Amphibia Anura Ranidae), near Rome

Short Note Grano & Cattaneo 2015

(Latium, Italy). Biodiversity Journal 2015, 5 (2): 213216. Hanselmann, R., Rodriguez, A., Lampo, M., FajardoRamos, L., Aguirre, A.A., Kilpatrick, A.M., Rodriguez, J.P. & Daszak, P. (2004): Presence of an emerging pathogen of amphibians in introduced bullfrogs Rana catesbeiana in Venezuela. Biological Conservation 120 (1): 115-119. Lambertz, M., Schmied, H. (2010): An ingrown ground beetle in the middle ear cavity of a North American bullfrog, Lithobates catesbeianus. Salamandra 46 (3): 185-186. Lanza, B. (1983): Anfibi, Rettili. Guida per il riconoscimento delle specie animali delle acque interne italiane. Consiglio Nazionale delle Ricerche AQ/1/205. Lanza, B., Andreone, F., Bologna, M.A., Corti, C., Razzetti, E. (2007): Amphibia. Fauna d’Italia. Vol. XLII. Edizioni Calderini, Bologna. Lowe, S., Browne, M., Boudjelas, S., De Poorter, M. (2000): 100 of the World’s Worst Invasive Alien Species. A selection from the Global Invasive Species Database. Published by The Invasive Species Specialist Group (ISSG) a specialist group of the Species Survival Commission (SSC) of the World Conservation Union (IUCN). First published as special lift-out in Aliens 12, December 2000. Updated and reprinted version: November 2004. Mazzoni, R., Cunnigham, A.A., Daszak, P., Apolo, A., Perdomo, E., Speranza, G. (2003). Emerging Pathogen of Wild Amphibians in Frogs (Rana catesbeiana). Farmed for International trade. Emerging Infectious Diseases 9 (8): 995-998. Kats, L.B., Ferrer, R.P. (2003): Alien predators and amphibian declines: review of two decades of science and the transition to conservation. Diversity and Distributions 9: 99-110. Pizzuti Piccoli, A., Cattaneo, A. (2008): Rinvenimento di un esemplare di rana toro, Lithobates catesbeianus (Shaw, 1802) (Amphibia, Anura, Ranidae), in località Maccarese (Roma, Italia). Atti del Museo di Storia Naturale della Maremma 22: 119-122. Santos-Barrera, G., Hammerson, G., Hedges, B., Joglar, R., Inchaustegui, S., Kuangyang, L., Wenhao, C., Huiqing, G., Haitao, S., Diesmos, A., Iskandar, D., van Dijk, P.P., Matsui, M., Schimdt, B., Miaud, C. & Martìnez-Solano, I. (2009): Lithobates catesbeianus. The IUCN Red List of Threatened Species. Version 2014.3 www.iucnredlist.org Downloaded 09 February 2015.

Hyla

VOL. 2015., No.1, Str. 70- 75 ISSN: 1848-2007

Short Note Grano & Cattaneo 2015

Scali, S. (2010): Le specie alloctone in Italia: censimenti, invasività e piani d’azione. Memorie della Società Italiana di Scienze Naturali e del Museo Civico di Storia Naturale di Milano 36: 1-96. Snow, N.P., Witmer, G. (2010): American Bullfrogs as Invasive Species: A review of the introduction, subsequent problems, management options, and future directions. Proc. 24th Vertebr. Pest Conference. Published at Univ. of California, Davis. 2010. Pp. 8689.