Abstract
The genus Blanus Wagler, 1830 (Squamata, Amphisbaenia) contains seven fossorial species found in the East Mediterranean Basin. Recent molecular-based studies suggested that former B. strauchi (Turkish worm lizard) is divided into three species spread from Southern Anatolia to Levantine region: B. strauchi, B. aporus and B. alexandri. Although these species not only have highly similar morphological characters but also are genetically distinct, the ecological niche differentiations have not been studied yet. We aim to predict the suitable habitats for related Blanus species and to determine niche overlaps and niche differentiation by similarity and identity tests. The occurrence records were obtained from literature and our own field surveys. These occurrence locations were assessed in 30 arc-second resolution layer, compatible with bioclimatic parameters from World-Clim (www.worldclim.org). Suitable habitat prediction analyses were performed in MaxEnt and the pairwise niche overlap comparisons were made in ENMTools. Our results show that precipitation and temperature dynamics may have an influence on the vegetation types, which provide suitable habitats for these species. Even in the most conservative model, where B.strauchi was designated as the ancestral species, the predicted distribution area was larger than the actual one. The niche overlap analysis confirms that the ecological differentiations among these taxa are valid. This result is in agreement with a previous molecular-based study. We speculate that the Messinian Salinity Crisis had an effect on precipitation and temperature dynamics and niche differentiation among the worm lizards, potentially contributing to species formation.
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References
Ahmadzadeh F, Flecks M, Carretero MA, Böhme W, Ilgaz Ç, Engler JO, Harris DJ, Üzüm N, Rödder D (2013a) Rapid lizard radiation lacking niche conservatism: ecological diversification within a complex landscape. J Biogeogr 40:1807–1818. https://doi.org/10.1111/jbi.12121
Ahmadzadeh F, Flecks M, Rödder D, Böhme W, Ilgaz Ç, Harris DJ, Engler JO, Üzüm N, Carretero MA (2013b) Multiple dispersal out of Anatolia: biogeography and evolution of oriental green lizards. Biol J Linn Soc 110:398–408. https://doi.org/10.1111/bij.12129
Albert EM, Fernandez A (2009) Evidence of cryptic speciation in a fossorial reptile: description of a new species of Blanus (Squamata: Amphisbaenia: Blanidae) from the Iberian Peninsula. Zootaxa 2234:56–68. https://doi.org/10.11646/zootaxa.2234.1.4
Alexander AA (1966) Taxonomy and variation of Blanus strauchi (Amphisbaenia, Reptilia). Copeia 1966(2):205–224. https://doi.org/10.2307/1441127
Amr ZS, Shehab A, Baker MA (2007) Recent observations on the herpetofauna of Syria with notes on trade in reptiles. Herpetozoa 20:21–26
Baran İ (1977) Türkiye’de Blanus strauchi Bedriaga 1884 türünün taksonomisi. Doğa Bilim Dergisi TÜBİTAK Ankara 1:192–196
Baran İ, Kumlutaş Y, Olgun K, Ilgaz Ç, Kaska Y (2001) The herpetofauna of the vicinity of Silifke. Turk J Zool 25:245–249
Baran İ, Kumlutaş Y, Tok CV, Ilgaz Ç, Avcı A, Özdemir A, Tosunoğlu M, İret F (2006) Güneydoğu Anadolu bölgesinin herpetofaunasının araştırılması. TÜBITAK Bilimsel ve Teknik Araştırma Kurumu, Temel Bilimler Araştırma Grubu, No: TBAG-2407 (104T017) Project Report, Ankara
Barve N, Barve V, Jiménez-Valverde A, Lira-Noriega A, Maher SP, Peterson AT, Soberón J, Villalobos F (2011) The crucial role of the accessible area in ecological niche modeling and species distribution modeling. Ecol Model 222:1810–1819. https://doi.org/10.1016/j.ecolmodel.2011.02.011
Bellati A, Carranza S, Garcia-Porta J, Fasola M, Sindaco R (2015) Cryptic diversity within the Anatololacerta species complex (Squamata: Lacertidae) in the Anatolian peninsula: evidence from a multi-locus approach. Mol Phylogenet Evol 82:219–233. https://doi.org/10.1016/j.ympev.2014.10.003
Brown JL (2014) SDM toolbox: a python-based GIS toolkit for landscape genetic, biogeographic and species distribution model analyses. Methods Ecol Evol 5:694–700. https://doi.org/10.1111/2041-210X.12200
Budak A, Tok CV, Mermer A (1998) A report on reptiles collected from Kumluca-Kalkan (Antalya), Turkey. Turk J Zool 22:158–190
Candan K, Kankılıç T, Güçlü Ö, Kumlutaş Y, Durmuş SH, Lymberakis P, Poulakakis N, Ilgaz Ç (2016) First assessment on the molecular phylogeny of Anatololacerta (Squamata, Lacertidae) distributed in southern Anatolia: insights from mtDNA and nDNA markers. Mitochondrial DNA A 27:2285–2292. https://doi.org/10.3109/19401736.2014.987238
Ceríaco LM, Bauer AM (2018) An integrative approach to the nomenclature and taxonomic status of the genus Blanus Wagler, 1830 (Squamata: Blanidae) from the Iberian Peninsula. J Nat Hist 52:849–880. https://doi.org/10.1080/00222933.2017.1422283
Cunningham RB, Lindenmayer DB, Crane M, Michael D, MacGregor C (2007) Reptile and arboreal marsupial response to replanted vegetation in agricultural landscapes. Ecol Appl 17:609–619
Doğaç M (1998) A study on the herpetofauna of Honaz Mountain (Denizli). MSc, Dokuz Eylül University, İzmir, Turkey
Ege O, Yakın BY, Tok CV (2015) Herpetofauna of the Lake District around Burdur. Turk J Zool 39:1164–1168. https://doi.org/10.3906/zoo-1502-7
Elith J, Phillips SJ, Hastie T, Dudík M, Chee YE, Yates CJ (2011) A statistical explanation of MaxEnt for ecologists. Divers Distrib 17:43–57. https://doi.org/10.1111/J.1472-4642.2010.00725.X
Fattahi R, Ficetola GF, Rastegar-Pouyani N, Avcı A, Kumlutaş Y, Ilgaz Ç, Yousefkhani SSH (2014) Modelling the potential distribution of the bridled skink, Trachylepis vittata (Olivier, 1804), in the Middle East. Zool Middle East 60:208–216. https://doi.org/10.1080/09397140.2014.944428
Fauquette S, Suc J-P, Bertini A, Popescu S-M, Warny S, Bachiri Taoufiq N, Perez Villa M-J, Chikhi H, Feddi N, Subally D, Clauzon G, Ferrier J (2006) How much did climate force the Messinian salinity crisis? Quantified climatic conditions from pollen records in the Mediterranean region. Palaeogeogr Palaeoclimatol Palaeoecol 238:281–301
Göçmen B, Disi AM, Yıldız MZ (2008) On the occurrence of Blanus strauchi aporus Werner, 1898 and Chalcides guentheri Boulenger, 1887 (Reptilia) in the Mediterranean ecozone of Syria. Zool Middle East 43:69–74. https://doi.org/10.1080/09397140.2008.10638270
Güçlü Ö, Candan K, Kankiliç T, Kumlutaş Y, Durmuş SH, Poulakakis N, Ilgaz Ç (2014) Phylogeny of Trachylepis sp. (Reptilia) from Turkey inferred from mtDNA sequences. Mitochondrial DNA 25:456–463. https://doi.org/10.3109/19401736.2013.814108
Gül S, Kumlutaş Y, Ilgaz Ç (2015) Climatic preferences and distribution of 6 evolutionary lineages of Typhlops vermicularis Merrem, 1820 in Turkey using ecological niche modeling. Turk J Zool 39:235–243. https://doi.org/10.3906/zoo-1311-9
Gül S, Kumlutaş Y, Ilgaz Ç (2016) Predicted distribution patterns of Pelias kaznakovi (Nikolsky, 1909) in the Caucasus hotspot with a new locality record from Turkey. Russ J Herpetol 23. https://doi.org/10.30906/1026-2296-2016-23-3-224-230
Heidari N (2019) Ecological niche differentiation between Acanthodactylus micropholis and A. khamirensis (Sauria: Lacertidae) in southern Iran. Zoologia (Curitiba) 36:1–5. https://doi.org/10.3897/zoologia.36.e27357
Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978. https://doi.org/10.1002/joc.1276
Jablonski D, Sadek RA (2019) The species identity and biogeography of Blanus (Amphisbaenia: Blanidae) in Lebanon. Zool Middle East 65:208–214. https://doi.org/10.1080/09397140.2019.1604471
Jezkova T, Wiens JJ (2018) Testing the role of climate in speciation: new methods and applications to squamate reptiles (lizards and snakes). Mol Ecol 27:2754–2769. https://doi.org/10.1111/mec.14717
Kapli P, Botoni D, Ilgaz Ç, Kumlutaş Y, Avcı A, Rastegar-Pouyani N, Poulakakis N (2013) Molecular phylogeny and historical biogeography of the Anatolian lizard Apathya (Squamata, Lacertidae). Mol Phylogenet Evol 66:992–1001. https://doi.org/10.1016/j.ympev.2012.12.002
Klausmeyer KR, Shaw MR (2009) Climate change, habitat loss, protected areas and the climate adaptation potential of species in Mediterranean ecosystems worldwide. PLoS One 4:1–9. https://doi.org/10.1371/journal.pone.0006392
Kornilios P, Ilgaz Ç, Kumlutaş Y, Lymberakis P, Moravec J, Sindaco R, Rastegar-Pouyani N, Afroosheh M, Giokas S, Fraguedakis-Tsolis S (2012) Neogene climatic oscillations shape the biogeography and evolutionary history of the Eurasian blindsnake. Mol Phylogenet Evol 62:856–873. https://doi.org/10.1016/j.ympev.2011.11.035
Kotsakiozi P, Jablonski D, Ilgaz Ç, Kumlutaş Y, Avcı A, Meiri S, Itescu Y, Kukushkin O, Gvoždík V, Scillitani G, Roussos S, Jandzik D, Kasapidis P, Lymberakis P, Poulakakis N (2018) Multilocus phylogeny and coalescent species delimitation in Kotschy’s gecko, Mediodactylus kotschyi: hidden diversity and cryptic species. Mol Phylogenet Evol 125:177–187. https://doi.org/10.1016/j.ympev.2018.03.022
Kozak KH, Graham CH, Wiens JJ (2008) Integrating GIS-based environmental data into evolutionary biology. Trends Ecol Evol 23:141–148. https://doi.org/10.1016/j.tree.2008.02.001
Kucharzewski C (2015) Herpetologische reiseeindrücke aus der Südwest-Türkei. Sauria 37:3–15
Kumlutaş Y, Ilgaz Ç, Durmuş SH (2001) Herpetofauna of Spil Mountain (Manisa) and its vicinity: Results of field surveys. Anadolu Univ J Sci Tech 2:63–66
Kumlutaş Y, Öz M, Durmuş SH, Tunç MR, Özdemir A, Düşen S (2004) On some lizard species of the western Taurus range. Turk J Zool 28:225–236
Mulder J (1995) Herpetological observations in Turkey (1987-1995). Deinsea 2:51–66
Mutlu HS, Ayaz D (2012) Ege Bölgesi’nde Yaşayan Blanus strauchi (Bedriaga, 1884) (Amphisbaenia, Blanidae) Populasyonlarının Taksonomisi. Anadolu Doğa Bilimleri Dergisi 3:41–51
Nakazato T, Warren DL, Moyle LC (2010) Ecological and geographic modes of species divergence in wild tomatoes. Am J Bot 97:680–693. https://doi.org/10.3732/ajb.0900216
Orszag-Sperber F, Rouchy JM, Blanc-Valleron MM (2000) La transition Messinien–Pliocène en Méditerranée orientale (Chypre): la période du Lago-Mare et sa signification. C R Acad Sci IIA Earth Planet Sci 331:483–490. https://doi.org/10.1016/S1251-8050(00)01433-6
Peterson AT (2011) Ecological niche conservatism: a time-structured review of evidence. J Biogeogr 38:817–827. https://doi.org/10.1111/j.1365-2699.2010.02456.x
Phillips SJ, Dudík M, Schapire RE (2017) Maxent software for modeling species niches and distributions (Version 3.4. 1). Biodiversity Informatics
Pontarp M, Wiens JJ (2017) The origin of species richness patterns along environmental gradients: uniting explanations based on time, diversification rate and carrying capacity. J Biogeogr 44:722–735. https://doi.org/10.1111/jbi.12896
R Core Team (2018) R: a language and environment for statistical computing, R foundation for statistical computing. R Core Team, Vienna, p 2018
Rajabizadeh M, Nagy ZT, Adriaens D, Avcı A, Masroor R, Schmidtler J, Nazarov R, Esmaeili HR, Christiaens J (2016) Alpine-Himalayan orogeny drove correlated morphological, molecular, and ecological diversification in the Persian dwarf snake (Squamata: Serpentes: Eirenis persicus). Zool J Linn Soc 176:878–913. https://doi.org/10.1111/zoj.12342
Raxworthy CJ, Ingram CM, Rabibisoa N, Pearson RG (2007) Applications of ecological niche modeling for species delimitation: a review and empirical evaluation using day geckos (Phelsuma) from Madagascar. Syst Biol 56:907–923. https://doi.org/10.1080/10635150701775111
Rissler LJ, Apodaca JJ, Weins J (2007) Adding more ecology into species delimitation: Ecological niche models and phylogeography help define cryptic species in the black salamander (Aneides flavipunctatus). Syst Biol 56(6):924–942. https://doi.org/10.1080/10635150701703063
Sarıkaya B, Yıldız MZ, Sezen G (2017) Adana ilinin herpetofaunası. Kommagene Biyoloji Dergisi 1:1–11. https://doi.org/10.31594/commagene.391784
Seifan M, Zohar Y, Werner YL (2016) Reptile distribution may identify terrestrial islands for conservation: the Levant’s ‘Arava Valley as a model. J Nat Hist 50:2783–2801. https://doi.org/10.1080/00222933.2016.1205154
Sindaco R, Kornilios P, Sacchi R, Lymberakis P (2014) Taxonomic reassessment of Blanus strauchi (Bedriaga, 1884) (Squamata: Amphisbaenia: Blanidae), with the description of a new species from south-East Anatolia (Turkey). Zootaxa 3795:311–326. https://doi.org/10.11646/zootaxa.3795.3.6
Skourtanioti E, Kapli P, Ilgaz Ç, Kumlutaş Y, Avcı A, Ahmadzadeh F, Crnobrnja-Isailović J, Gherghel I, Lymberakis P, Poulakakis N (2016) A reinvestigation of phylogeny and divergence times of the Ablepharus kitaibelii complex (Sauria, Scincidae) based on mtDNA and nuDNA genes. Mol Phylogenet Evol 103:199–214. https://doi.org/10.1016/j.ympev.2016.07.005
Swets JA (1988) Measuring the accuracy of diagnostic systems. Science 240:1285–1293. https://doi.org/10.1126/science.3287615
Tamar K, Carranza S, Sindaco R, Moravec J, Meiri S (2014) Systematics and phylogeography of Acanthodactylus schreiberi and its relationships with Acanthodactylus boskianus (Reptilia: Squamata: Lacertidae). Zool J Linn Soc 172:720–739. https://doi.org/10.1111/zoj.12170
Tamar K, Carranza S, In den Bosch H, Sindaco R, Moravec J, Meiri S (2015) Hidden relationships and genetic diversity: molecular phylogeny and phylogeography of the Levantine lizards of the genus Phoenicolacerta (Squamata: Lacertidae). Mol Phylogenet Evol 91:86–97. https://doi.org/10.1016/j.ympev.2015.05.002
Tok CV, Tosunoğlu M, Ayaz D, Çiçek K, Mutlu HS (2012) New records of the Anatolian worm lizard, Blanus strauchi (Bedriaga, 1884), from Turkey (Squamata: Amphisbaenia: Blanidae). Herpetozoa 24:107–111
Uğurtaş İH, Yıldırımhan HS, Öz M (2000) Herpetofauna of the eastern region of the Amanos Mountains (Nur). Turk J Zool 24:257–262
Veith M, Göçmen B, Sotiropoulos K, Eleftherakos K, Lötters S, Godmann O, Karış M, Oğuz A, Ehl S (2020) Phylogeographic analyses point to long-term survival on the spot in micro-endemic Lycian salamanders. PLoS One 15(1):1–22. https://doi.org/10.1371/journal.pone.0226326
Walther GR, Post E, Convey P, Menzel A, Parmesan C, Beebee TJ, Fromentin JM, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416:389. https://doi.org/10.1038/416389a
Warren DL, Glor RE, Turelli M (2010) ENMTools: a toolbox for comparative studies of environmental niche models. Ecography 33:607–611. https://doi.org/10.1111/j.1600-0587.2009.06142.x
Yakalı EN (2015) Blanus (Reptilia: Amphisbaenia) cinsinin Diyarbakır il sınırları içerisindeki dağılışı ve taksonomisi. MSc Thesis, Dicle University, Diyarbakır, Turkey
Yıldız MZ, Akman B, Göçmen B, Yalçinkaya D (2009) New locality records for the Turkish worm lizard, Blanus strauchi aporus (Werner, 1898) (Sauria: Amphisbaenidae) in Southeast Anatolia, Turkey. North-West J Zool 5:379–385
Yıldız MZ, Sarıkaya B, Bozkurt MA (2019) The herpetofauna of the province of Hatay (East Mediterranean Turkey). Biol Divers Conserv 12:197–205. https://doi.org/10.5505/biodicon.2019.93685
Yousefkhani HSS, Javaheri Tehrani S, Moodi B, Gül S (2016a) Distribution patterns and habitat suitability for three species of the genus Hyla Laurenti, 1768 in the Western Palearctic. Turk J Zool 40:257–273. https://doi.org/10.3906/zoo-1507-38
Yousefkhani HSS, Mirshamsi O, Ilgaz Ç, Kumlutaş Y, Avcı A (2016b) Ecological niche divergence between Trapelus ruderatus (Olivier, 1807) and T. persicus (Blanford, 1881) (Sauria: Agamidae) in the Middle East. Asian Herpetol Res 7:96–102. https://doi.org/10.16373/j.cnki.ahr.150032
Yousefkhani SSH, Rastegar-Pouyani E, Ilgaz Ç, Kumlutaş Y, Avcı A, Wink M (2019) Evidences for ecological niche differentiation on the Anatolian lizard (Apathya cappadocica ssp.) (Reptilia: Lacertidae) in western Asia. Biologia 74:1661–1667. https://doi.org/10.2478/s11756-019-00273-4
Zaloğlu Ş (1968) Taxonomy of the genus Blanus (Amphisbaenidae, Reptilia) in Turkey. Science Reprint Faculty of Science. Ege University, İzmir, pp 1–15
Zhao Q, Zhang H, Wei J (2019) Climatic niche comparison across a cryptic species complex. PeerJ 7:e7042. https://doi.org/10.7717/peerj.7042
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Authors thank Dr. Alexey Yanchukov and Can Elverici for their important suggestions.
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Şahin, M.K., Candan, K., Yildirim Caynak, E. et al. Ecological niche divergence contributes species differentiation in worm lizards (Blanus sp.) (Squamata: Amphisbaenia: Blanidae) in Mediterranean part of Anatolian peninsula and the Levantine region. Biologia 76, 525–532 (2021). https://doi.org/10.2478/s11756-020-00548-1
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DOI: https://doi.org/10.2478/s11756-020-00548-1