Morphological and ecological divergence in two populations of European glass lizard, <i>Pseudopus apodus</i> (Squamata: Anguidae)

Olga Jovanović Glavaš; Paula Počanić; Vanja Lovrić; Lorena Derežanin; Zoran Tadić; Duje Lisičić

doi:10.24272/j.issn.2095-8137.2020.025

Volume 41 Issue 2

Mar. 2020

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Olga Jovanović Glavaš, Paula Počanić, Vanja Lovrić, Lorena Derežanin, Zoran Tadić, Duje Lisičić. Morphological and ecological divergence in two populations of European glass lizard, Pseudopus apodus (Squamata: Anguidae). Zoological Research, 2020, 41(2): 172-181. doi: 10.24272/j.issn.2095-8137.2020.025

Citation:

Olga Jovanović Glavaš, Paula Počanić, Vanja Lovrić, Lorena Derežanin, Zoran Tadić, Duje Lisičić. Morphological and ecological divergence in two populations of European glass lizard, Pseudopus apodus (Squamata: Anguidae). Zoological Research, 2020, 41(2): 172-181. doi: 10.24272/j.issn.2095-8137.2020.025

Citation:

Olga Jovanović Glavaš, Paula Počanić, Vanja Lovrić, Lorena Derežanin, Zoran Tadić, Duje Lisičić. Morphological and ecological divergence in two populations of European glass lizard, Pseudopus apodus (Squamata: Anguidae). Zoological Research, 2020, 41(2): 172-181. doi: 10.24272/j.issn.2095-8137.2020.025

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Morphological and ecological divergence in two populations of European glass lizard, Pseudopus apodus (Squamata: Anguidae)

doi: 10.24272/j.issn.2095-8137.2020.025

1.
Department of Biology, University of Osijek, Osijek 31000, Croatia
2.
Department of Animal Physiology, Faculty of Science, University of Zagreb, Zagreb 10000, Croatia

Funds: This work was partly supported through grant 119-0000000-1285 of the Ministry of Science of the Republic of Croatia to Z.T.

More Information

Corresponding author: E-mail: duje.lisicic@biol.pmf.hr; E-mail: duje.lisicic@biol.pmf.hr
Received Date: 2019-09-20
Publish Date: 2020-03-01

Abstract

Abstract

The European glass lizard, Pseudopus apodus (Pallas, 1775), is a large, legless lizard with wide distribution across south-eastern Europe and eastern and central Asia. To date, morphological diversification among populations on a geographically small scale has not yet been reported in this lizard. Thus, we investigated the morphological variations and corresponding differences in habitat utilization between two populations of P. apodus inhabiting the same biogeographical zone within a relatively close geographic area. We hypothesized that minor differences in habitat could induce a significant level of morphological differentiation, thus indicating morphological plasticity in this species on a small geographical scale. We sampled 164 individuals (92 from the Croatian mainland and 72 from the island of Cres). Results showed that P. apodus indeed exhibited morphological differences between populations in the same biogeographical zone within a relatively close geographic area, with the Cres Island individuals being generally larger than the individuals from the mainland. Some ecological characteristics were similar in both populations (e.g., soil temperature, distance to hiding place), whereas others were distinct (e.g., air temperature and humidity). In addition, vegetation cover differed between the two sites, with more vegetation present on the mainland than on the island. Furthermore, the Cres Island population showed clear sexual dimorphism, which was absent in the mainland population.
- Mediterranean,
- Morphology,
- Sauria,
- Sexual dimorphism

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References(68)

References

[1]	Abe AS. 1995. Estivation in South American amphibians and reptiles. Brazilian Journal of Medical and Biological Research, 28(11–12): 1241−1247.
[2]	Alekperov AM. 1978. Amphibians and reptiles of Azerbaijan. Elm, Baku.
[3]	Arnold EN. 2002. Reptiles and Amphibians of Europe. 2^nd ed. Princeton: Princeton University Press.
[4]	Aubret F. 2015. Island colonisation and the evolutionary rates of body size in insular neonate snakes. Heredity, 115(4): 349−356. doi: 10.1038/hdy.2014.65
[5]	Bakaloudis DE, Vlachos CG, Holloway GJ. 1998. Habitat use by short-toed eagles Circaetus gallicus and their reptilian prey during the breeding season in Dadia Forest (north-eastern Greece). Journal of Applied Ecology, 35(6): 821−828.
[6]	Blanckenhorn WU. 2000. The evolution of body size: what keeps organisms small?. The Quarterly Review of Biology, 75(4): 385−407. doi: 10.1086/393620
[7]	Bogdanov OP. 1986. Presmikayushchiesya Srednei Azii. Tashkent, Uzbekistan, Ukituvchi. (in Russian)
[8]	Bohonak AJ, van der Linde K. 2004(2016-03-28). RMA: software for reduced major axis regression, Java version. http://www.kimvdlinde.com/professional/rma.html.
[9]	Buhlmann KA. 1995. Habitat use, terrestrial movements, and conservation of the turtle, Deirochelys reticularia in Virginia. Journal of Herpetology, 29(2): 173−181. doi: 10.2307/1564554
[10]	Carretero M, Znari M, Macé J, Harris DJ. 2005. Morphological divergence among populations of Testudo graeca from west-central Morocco. Animal Biology, 55(3): 259−279. doi: 10.1163/1570756054472854
[11]	Case TJ. 1978. A general explanation for insular body size trends in terrestrial vertebrates. Ecology, 59(1): 1−18. doi: 10.2307/1936628
[12]	Christiansen S, Wroe S. 2007. Bite forces and evolutionary adaptations to feeding ecology in carnivores. Ecology, 88(2): 347−358. doi: 10.1890/0012-9658(2007)88[347:BFAEAT]2.0.CO;2
[13]	Çiçek K, Tok CV, Hayretdağ S, Ayaz D. 2014. Data on the food composition of European glass lizard, Pseudopus apodus (Pallas, 1775) (Squamata: Anguidae) from Canakkale (Western Anatolia, Turkey). Acta Zoologica Bulgarica, 66(3): 433−436.
[14]	Cooper Jr W, Pérez-Mellado V, Hawlena D. 2009. Morphological traits affect escape behaviour of the Balearic lizards (Podarcis lilfordi). Amphibia-Reptilia, 30(4): 587−592. doi: 10.1163/156853809789647167
[15]	Corti C, Masseti M, Delfino M, Pérez-Mellado V. 1999. Man and herpetofauna of the Mediterranean islands. Revista Española de Herpetologia, 13: 83−100.
[16]	Dewar EW, Crocker CA, Bauchiero AV, Livingstone JP. 2015. Is skull shape related to aggressive displays in Pinnipeds?. FASEB Journal, 29(S1): 696−698.
[17]	Dollion AY, Measey GJ, Cornette R, Carne L, Tolley KA, da Silva JM, Boistel R, Fabre AC, Herrel A. 2017. Does diet drive the evolution of head shape and bite force in chameleons of the genus Bradypodion?. Functional Ecology, 31(3): 671−684. doi: 10.1111/1365-2435.12750
[18]	Dumančić D. 1992. Improvement of lawn production in Mediterranean as a precondition for sheep and goat farming. Agronomski Glasnik, 1–88: 105−111.
[19]	Estes J, Crooks K, Holt RD. 2001. Predators, ecological role of. In: Levin SA. Encyclopedia of Biodiversity. San Diego: Academic Press, 857–878.
[20]	Foster JB. 1964. Evolution of mammals on islands. Nature, 202(4929): 234−235. doi: 10.1038/202234a0
[21]	Georgiev D, Raichev E. 2009. A record of Horned viper Vipera ammodytes (L.) in the diet of the Stone marten Martes foina (Erxl.) (Mammalia: Mustelidae) in Bulgaria. ZooNotes, 5: 1−2.
[22]	Herrel A, Van Damme R, Vanhooydonck B, De Vree F. 2001. The implications of bite performance for diet in two species of lacertid lizards. Canadian Journal of Zoology, 79(4): 662−670. doi: 10.1139/z01-031
[23]	Herrel A, Vanhooydonck B, Van Damme R. 2004a. Omnivory in lacertid lizards: adaptive evolution or constraint?. Journal of Evolutionary Biology, 17(5): 974−984. doi: 10.1111/j.1420-9101.2004.00758.x
[24]	Herrel A, Vanhooydonck B, Joachim R, Irschick DJ. 2004b. Frugivory in polychrotid lizards: effects of body size. Oecologia, 140(1): 160−168. doi: 10.1007/s00442-004-1558-7
[25]	Herrel A, Huyghe K, Vanhooydonck B, Backeljau T, Breugelmans K, Grbac I, Van Damme R, Irschick DJ. 2008. Rapid large-scale evolutionary divergence in morphology and performance associated with exploitation of a different dietary resource. Proceedings of the National Academy of Sciences of the United States of America, 105(12): 4792−4795. doi: 10.1073/pnas.0711998105
[26]	Higham TE, Russell AP, Zani PA. 2013. Integrative biology of tail autotomy in lizards. Physiological and Biochemical Zoology, 86(6): 603−610. doi: 10.1086/673875
[27]	Horvatić S. 1963. Biogeographical position and articulation of our coast in the light of modern phytocenological research. Acta Botanica Croatica, 22: 27−81.
[28]	Hurston H, Voith L, Bonanno J, Foufopoulos J, Pafilis P, Valakos E, Anthony N. 2009. Effects of fragmentation on genetic diversity in island populations of the Aegean wall lizard Podarcis erhardii (Lacertidae, Reptilia). Molecular Phylogenetics and Evolution, 52(2): 395−405. doi: 10.1016/j.ympev.2009.03.028
[29]	Itescu Y, Schwarz R, Donihue CM, Slavenko A, Roussos SA, Sagonas K, Valakos ED, Foufopoulos J, Pafilis P, Meiri S. 2018. Inconsistent patterns of body size evolution in co-occurring island reptiles. Journal of Biogeography, 27(5): 538−550.
[30]	Jablonski D. 2018. Male-male combat in Pseudopus apodus (Reptilia: Anguidae). Russian Journal of Herpetology, 25(4): 293−298. doi: 10.30906/1026-2296-2018-25-4-293-298
[31]	Jandzik D, Jablonski D, Zinenko O, Kukushkin OV, Moravec J, Gvoždík V. 2018. Pleistocene extinctions and recent expansions in an anguid lizard of the genus Pseudopus. Zoologica Scripta, 47(1): 21−32. doi: 10.1111/zsc.12256
[32]	Janzen FJ. 1993. An experimental analysis of natural selection on body size of hatchling turtles. Ecology, 74(2): 332−341. doi: 10.2307/1939296
[33]	Jones KE, Ruff CB. 2011. Male-male combat drives bite force evolution in the absence of mastication. FASEB Journal, 25(1): 867.
[34]	Kukushkin OV, Dovgal IV. 2018. Sexual dimorphism in Pseudopus apodus (Reptilia: Sauria: Anguidae) from the Steppe Crimea. Ecologica Montenegrina, 19: 1−21.
[35]	Lomolino MV. 2005. Body size evolution in insular vertebrates: generality of the island rule. Journal of Biogeography, 32(10): 1683−1699. doi: 10.1111/j.1365-2699.2005.01314.x
[36]	Losos JB. 1990. Ecomorphology, performance capability, and scaling of West Indian Anolis lizards: an evolutionary analysis. Ecological Monographs, 60(3): 369−388. doi: 10.2307/1943062
[37]	Losos JB, Creer DA, Glossip D, Goellner R, Hampton A, Roberts G, Haskell N, Taylor P, Ettling J. 2000. Evolutionary implications of phenotypic plasticity in the hindlimb of the lizard Anolis sagrei. Evolution, 54(1): 301−305.
[38]	Meiri S. 2008. Evolution and ecology of lizard body sizes. Global Ecology and Biogeography, 17(6): 724−734. doi: 10.1111/j.1466-8238.2008.00414.x
[39]	Nowak RM. 1991. Walker's Mammals of the World. 5^th ed. Baltimore: The Johns Hopkins University Press.
[40]	Obst FJ. 1978. On geographical variability of Scheltopusik, Ophisaurus apodus (Pallas). Zoologische Abhandlungen Staatliches Museum für Tierkunde in Dresden, 35: 129−140.
[41]	Obst FJ. 1981. Ophisaurus apodus (Pallas, 1775)-Scheltopusik. In: Handbuch der Reptilien und Amphibien Europas, vol. 1. Echsen (Sauria). Akademische Verlags gesellschaft, Wiesbaden, 259–274. (in German)
[42]	Owens IP, Scott SN, Robinson SI, Clegg SM, Kikkawa J. 2006. Large body size in island-dwelling passerines: the roles of insular specialization, niche expansion and ecological release. Acta Zoologica Sinica, 52(S1): 262−266.
[43]	Pafilis P, Meiri S, Foufopoulos J, Valakos E. 2009. Intraspecific competition and high food availability are associated with insular gigantism in a lizard. Naturwissenschaften, 96(9): 1107−1113. doi: 10.1007/s00114-009-0564-3
[44]	Palkovacs EP. 2003. Explaining adaptive shifts in body size on islands: a life history approach. Oikos, 103(1): 37−44. doi: 10.1034/j.1600-0706.2003.12502.x
[45]	Peig J, Green AJ. 2009. New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos, 118(12): 1883−1891. doi: 10.1111/j.1600-0706.2009.17643.x
[46]	Rifai L, Baker MA, Al Shafei D, Disi AM, Manhasneh A, Amr Z. 2005. Pseudopus apodus (Pallas, 1775) from Jordan, with notes on its ecology (Sqamata: Sauria: Anguidae). Herpetozoa, 18(3–4): 133−140.
[47]	Ripple WJ, Beschta RL. 2004. Wolves and the ecology of fear: can predation risk structure ecosystems?. BioScience, 54(8): 755−766. doi: 10.1641/0006-3568(2004)054[0755:WATEOF]2.0.CO;2
[48]	Sagonas K, Pafilis P, Lymberakis P, Donihue CM, Herrel A, Valakos ED. 2014. Insularity affects head morphology, bite force and diet in a Mediterranean lizard. Biological Journal of the Linnean Society, 112(3): 469−484. doi: 10.1111/bij.12290
[49]	Santana SE, Dumont ER, Davis JL. 2010. Mechanics of bite force production and its relationship to diet in bats. Functional Ecology, 24(4): 776−784. doi: 10.1111/j.1365-2435.2010.01703.x
[50]	Sears MW, Angilletta Jr MJ. 2003. Life-history variation in the sagebrush lizard: phenotypic plasticity or local adaptation?. Ecology, 84(6): 1624−1634. doi: 10.1890/0012-9658(2003)084[1624:LVITSL]2.0.CO;2
[51]	Shcherbak NN. 1966. Amphibians and Reptiles of the Crimea (Herpetologia Taurica). Kiev: Naukova Dumka. (in Russian).
[52]	Soulé ME, Estes JA, Berger J, del Rio CM. 2003. Ecological effectiveness: conservation goals for interactive species. Conservation Biology, 17(5): 1238−1250. doi: 10.1046/j.1523-1739.2003.01599.x
[53]	Storey KB. 2001. Turning down the fires of life: Metabolic regulation of hibernation and estivation. In: Storey KB. Molecular Mechanisms of Metabolic Arrest. Oxford: BIOS Scientific Publishers, 1–21.
[54]	Sušić G, Radek V. 2007. Biodiversity through ponds of Cres Island. Istraživačko-edukacijski centar za zaštitu prirode Eko Centar Insulae, Beli. (in Croatian)
[55]	Telenchev I, Simeonovska-Nikolova D, Natchev N, Tzankov N. 2015. A preliminary study on the habitat selection of European glass lizard (Pseudopus apodus) in southeast Bulgaria. In: First National Conference of Biotechnology. Sofia, 2014.
[56]	Telenchev I, Simeonovska-Nikolova D, Tzonev R. 2017. Habitat use and activity of European glass lizard, Pseudopus apodus (Pallas, 1775), in southeastern Bulgaria. Turkish Journal of Zoology, 41(2): 286−293.
[57]	Thomas R, Hedges SB. 1998. New anguid lizard (Diploglossus) from Cuba. Copeia, 1998(1): 97−103. doi: 10.2307/1447704
[58]	TIBCO Software Inc. 2018. Statistica (data analysis software system), version 13. http://tibco.com.
[59]	Tomašević Kolarov N, Ljubisavljević K, Polović L, Džukić G, Kalezić ML. 2010. The body size, age structure and growth pattern of the endemic Balkan Mosor rock lizard (Dinarolacerta mosorensis Kolombatović, 1886). Acta Zoologica Academiae Scientiarum Hungaricae, 56(1): 55−71.
[60]	Topić J. 2001. Vegetation (Flora) of Croatia. In: Lovstvo JJ. Croatia: Strossmayer University of Osijek, 105–124. (in Croatian)
[61]	Tutiš V, Kralj J, Radović D, Ćiković D, Barišić S. 2013. Red Data Book of Birds of Croatia. Republic of Croatia: Ministry of Environmental and Nature Protection, State Institute for Nature Protection.
[62]	Vervust B, Pafilis P, Valakos ED, Van Damme R. 2010. Anatomical and physiological changes associated with a recent dietary shift in the lizard Podarcis sicula. Physiological and Biochemical Zoology, 83(4): 632−642. doi: 10.1086/651704
[63]	Verwaijen D, Van Damme R, Herrel A. 2002. Relationships between head size, bite force, prey handling efficiency and diet in two sympatric lacertid lizards. Functional Ecology, 16(6): 842−850. doi: 10.1046/j.1365-2435.2002.00696.x
[64]	Vincent SE, Herrel A. 2007. Functional and ecological correlates of ecologically-based dimorphisms in squamate reptiles. Integrative and Comparative Biology, 47(2): 172−188. doi: 10.1093/icb/icm019
[65]	Werner EE, Gilliam JF. 1984. The ontogenetic niche and species interactions in size-structured populations. Annual Review of Ecology and Systematics, 15: 393−425. doi: 10.1146/annurev.es.15.110184.002141
[66]	Wikelski M. 2005. Evolution of body size in Galapagos marine iguanas. Proceedings of the Royal Society B: Biological Sciences, 272(1576): 1985−1993. doi: 10.1098/rspb.2005.3205
[67]	Wyckmans M, Van Wassenbergh S, Adriaens D, Van Damme R, Herrel A. 2007. Size-related changes in cranial morphology affect diet in the catfish Clariallabes longicauda. Biological Journal of the Linnean Society, 92(2): 323−334. doi: 10.1111/j.1095-8312.2007.00846.x
[68]	Zaninović K, Gajić-Čapka M, Perčec Tadić M, Vučetić M, Bajić A, Cindrić K, Cvitan L, Katušin Z, Kaučić D, Likso T, Lončar E, Lončar Ž, Mihajlović D, Pandžić K, Patarčić M, Srnec L, Vučetić V. 2008. Atlas of Croatia 1961–1990, 1971–2000. Zagreb: Meteorological and Hydrological Service of Croatia.