Skin morphology of five species of rock lizards of the genus Darevskia (Lacertidae, Squamata)
- Autores: Chernova O.F.1, Galoyan E.A.1, Ivlev Y.F.1
-
Afiliações:
- A. N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences
- Edição: Nº 4 (2024)
- Páginas: 460-467
- Seção: ZOOLOGY
- URL: https://cijournal.ru/1026-3470/article/view/647785
- DOI: https://doi.org/10.31857/S1026347024040049
- EDN: https://elibrary.ru/VHYVAS
- ID: 647785
Citar
Texto integral
Resumo
The microstructure of the tuberculate dorsal and lamellar ventral skin of the body in rock lizards of different ages (Darevskia raddei, D. nairensis, D. valentini, D. dahli, D. armeniaca) has been described for the first time. The thickness of the skin in the most xerophilic species (D. raddei) is less than that in the more hygrophilic species. Rock lizards have single or paired longitudinal skin folds that are not closed from the side, which stretch along the inner side of the scales to its distal edge. Small folds are also present in the lining of the squamous pocket; they consist of all layers of the skin and subcutaneous tissue. A large fold is able to completely block the cavity of the squamous pocket, the volume of which changes with the contraction of the subcutaneous muscle bundles reaching the bases of the scales. Small folds are also present on the scales of tuberous skin. In hygrophilic lizards (Zootoca vivipara), similar formations appear at later stages of postnatal ontogenesis than in rock lizards. The probable functional significance of the described skin structures is discussed.
Palavras-chave
Texto integral

Sobre autores
O. Chernova
A. N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences
Autor responsável pela correspondência
Email: olga.chernova.moscow@gmail.com
Rússia, Moscow, 119071
E. Galoyan
A. N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences
Email: olga.chernova.moscow@gmail.com
Rússia, Moscow, 119071
Yu. Ivlev
A. N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences
Email: olga.chernova.moscow@gmail.com
Rússia, Moscow, 119071
Bibliografia
- Гражданкин А. В. Особенности морфологии кожного покрова наземных рептилий в связи с их терморегуляцией // Зоол. журн. 1974. Т. 53. № 12. С. 1894–1897.
- Даревский И. C. Скальные ящерицы Кавказа: Систематика, экология и филогения полиморфной группы кавказских ящериц подрода Archaeolacerta / Зоол. ин-т. Л.: Наука. Ленингр. отд., 1967. 214 с.
- Даревский И. С., Гречко В. В., Куприянова Л. A. Ящерицы, размножающиеся без самцов // Природа. 2000. № 9. С. 131–133.
- Николаев О. Д., Белова Д. А., Новиковa Б. А., Симисa И. Б., Петросян Р. К., Аракелян М. С., Комарова В. А., Галоян Э. А. Особенности термобиологии партеногенетических скальных ящериц (Darevskia armeniaca и Darevskia unisexualis) и обоеполового вида Darevskia valentini (Lacertidae, Squamata) // Зоол. журн. 2021. Т. 100. № 11. С. 1214–1223. https://doi.org/10.31857/S0044513421090063
- Попов В. Л., Механика контактного взаимодействия и физика трения. От нанотрибологии до динамики землетрясений. М.: Физматлит, 2013. 352 с.
- Соколов В. Е., Даревский И. С., Котова Е. Л., Чернова О. Ф. Специализированные кожные органы такырной круглоголовки Phrynocephalus helioscopus (Reptilia. Squamata, Agamidae) // Зоол. журн. 1997. Т.70. № 4. С. 466–472.
- Соколов В. Е., Котова Е. Л., Чернова O. Ф., 1994. Кожные железы рептилий (Reptilia). Обзор исследований. М.: МЦНЕИ. С. 1–94.
- Соколов В. Е., Скурат Л. Н., Степанова Л. В., Шабадаш С. А. Руководство по изучению кожного покрова млекопитающих. М.: Наука, 1988. 278 с.
- Abramoff M. D., Magalhaes P. J., Ram S. J. Image Processing with ImageJ // Biophotonics International. 2004. V. 11. № 7. P. 36–42.
- Ahmadzadeh F., Flecks M., Carretero M. A., Mozaffari O., Böhme W., Engler J., Harris D. J., IIgaz C., Üzüm. N. Cryptic speciation patterns in Iranian rock lizards uncovered by integrative taxonomy // PloS ONE. 2013. V. 8. № 12. P. 1–17. https://doi.org/10.1371/journal.pone.0080563
- Akat E., Pombal V. F., Yenmiş M., Molist P., Megias M., Somuncu S., Vesely M., Anderson R., Ayaz D. Comparison of vertebrate skin structure at class level: A review // Anat. Rec. 2022. V. 305. № 12. P. 3543– 3608. https://doi.org/10.1002/ar.24908
- Alibardi L. Scale morphogenesis during embryonic development in the lizard Anolis lineatopus // J. Anat. 1996. V. 188. P. 713–725.
- Alibardi L. Morphogenesis of the digital pad lamellae in the embryo of the lizard Anolis lineatopus // J. Zool. 1997. V. 243. P. 47–56. https://doi.org/10.1111/j.1469-7998.1997.tb05755.x
- Alibardi L. Ultrastructure of the embryonic snake skin and putative role of histidine in the differentiation of the shedding complex // J. Morphol. 2002. V. 251. P. 149–168. https://doi.org/10.1002/jmor.1080
- Alibardi L. Adaptation to the land: The skin of reptiles in comparison to that of amphibians and endotherm amniotes // J. Exp. Zool. Part B. Mol. Dev. Evol. 2003. V. 298. № 1. P. 12–41. https://doi.org/10.1002/jez.b.24
- Alibardi L. Review: Cell biology of adhesive setae in gecko lizards // Zoology. 2009. V. 112. P. 403–424. https://doi.org/10.1016/j.zool.2009.03.005
- Alibardi L. Sauropsids cornification is based on corneous beta-proteins, a special type of keratin-associated corneous proteins of the epidermis // J. Exp. Zool. Part B. Mol. Dev. Evol. 2016. V. 326. № 6. P. 1–14. https://doi.org/10.1002/jez.b.22689
- Alibardi L. Keratinization and cornification are not equivalent processes but keratinization in fish and amphibians evolved into cornification in terrestrial vertebrates // Exp. Dermat. 2022. V. 31. № 5. P. 794–799. https://doi.org/10.1111/exd.14525
- Alibardi L., Thompson M. B. Epidermal differentiation in the developing scales of embryos of the Australian scincid lizard Lampropholis quicnenoti // J. Morphol. 1999. V. 241. P. 139–152. https://doi.org/10.1002/(SICI)1097-4687(199908)241:2<139::AID-JMOR4>3.0.CO;2-H.
- Alibardi L., Toni M., Cytochemical, biochemical and molecular aspects of the process of keratinization in the epidermis of reptilian scales // Prog. Histochem. Cytochem. 2006. V. 40. № 2. P. 73–134. https://doi.org/10.1016/j.proghi.2006.01.001
- Ananjeva N. B., Dilmuchamedov M., Matveyeva T. The skin sense organs of some iguanian lizards // J. Herpetol. 1991. V. 25. P. 186–199. https://doi.org/10.2307/1564647
- Araya-Donoso R., San Juan E., Tamburrino I., Lamborot M., Veloso C., Véliz D. Integrating genetics, physiology and morphology to study desert adaptation in a lizard species // J. Anim. Ecol. 2022. V. 91. № 6. P. 1148–1162. https://doi.org/10.1111/1365-2656.13546
- Arribas O. J. Phylogeny and relationships of the mountain lizards of Europe and Near East (Archaeolacerta Mertens, 1921, sensu lato) and their relationships among the Eurasian lacertid radiation // Russ. J. Herpetol. 1999. V. 6. № 1. P. 1–22.
- Breyer H. Über Hautsinnesorgane und Haftung bei Lacertilien // Zool. Jahr. 1929. Bd. 51. Abt. F. Anatomie. S. 549–581.
- Calvaresi M., Eckhart L., Alibardi L. The molecular organization of the beta-sheet region in Corneous betaproteins (beta-keratins) of sauropsids explains its stability and polymerization into filaments // J. Struct. Biol. 2016. V. 194. P. 282–291. https://doi.org/10.1016/j.jsb.2016.03.004
- Carver W. S., Sawyer R. H. Development and keratinization of the epidermis in the common lizard, Anolis carolinenesis // J. Exp. Zool. 1987. V. 243. P. 435–443. https://doi.org/ 10.1002/jez.1402430310
- Chang Ch., Wu P., Baker R. E., huong Ch.-M. Reptile scale paradigm: Evo-Devo pattern formation and regeneration // Int. J. Dev. Biol. 2009. V. 53. P. 813–826. https://doi.org/10.1387/ijdb.072556cc.
- Comans P., Buchberger G., Buchsbaum A., Baumgartner R., Koller A., Bauer S., Baumgartner W. Directional, passive liquid transport: the Texas horned lizard as a model for a biomimetic ‘liquid diode’ // J. R. Soc. Interface. 2015. V. 12. № 109. P. 20150415. https://doi.org/10.1098/rsif.2015.0415
- Comans P., Withers P. C., Esser F. J., Baumgartner W. Cutaneous water collection by a moisture-harvesting lizard, the thorny devil (Moloch horridus) // J. Exp. Biol. 2016. V. 219. № 21. P. 3473–3479. https://doi.org/10.1242/jeb.148791
- Cox C. L., Cox R. M. Evolutionary shifts in habitat aridity predict evaporative water loss across squamate reptiles // Evolution. 2015. V. 69. № 9. P. 2507–2516.
- Dhouailly D. A new scenario for the evolutionary origin of hair, feather, and avian scales // J. Anat. 2009. V. 214. № 4. P. 587−606. https://doi.org/10.1111/j.1469-7580.2008.01041.x.
- Dupoué A., Rutschmann A., Le Galliard J. F., Miles D. B., Clobert J., Devardo D. F., Brusch G. A. IV, Meylan S. Water availability and environmental temperature correlate with geographic variation in water balance in common lizards // Oecologia. 2017. V. 185. № 4. P. 561–571. https://doi.org/10.1007/s00442-017-3973-6.
- Flaxman B. A. Cell differentiation and its control in the vertebrate epidermis // Integrative and Comparative Biology (ICB). 1972. V. 12. № 1. P. 13−26. https://doi.org/10.1093/icb/12.1.13
- Gabelaia M., Adriaens D., Tarkhnishvili D. Phylogenetic signals in scale shape in Caucasian rock lizards (Darevskia species) // Zool. Anz. 2017. V. 268. P. 32–40. https://doi.org/10.1016/j.jcz.2017.04.004
- Galoyan E., Moskalenko V., Gabelaia M., Tarkhnishvili D., Spangenverg V. E., Shamkina A., Arakelyan M., Syntopy of two species of rock lizards (Darevskia raddei and Darevskia portschinskii) may not lead to hybridization between them // Zool. Anz. 2020. V. 288. P. 43–52. https://doi.org/10.1016/j.jcz.2020.06.007 https://sev-in.ru/sites/default/files/2023-08/Supplementary_to_Skin_morphology_of_rock_lizards.pdf.
- Irish F. J., Williams E. E., Seling E. Scanning electron microscopy of changes in epidermal structure occurring during the shedding cycle in squamate reptiles // J. Morph. 1988. V. 197. № 1. P. 105–126. https://doi.org/10.1002/jmor.1051970108
- Kandagel R., Elwan M., Abumdour M. Comparative ultrastructural-functional characterizations of the skin in three reptile species: Chalcides ocellatus, Uromastyx aegyptia aegyptia, and Psammophis schokari aegyptia (Forskål, 1775): Adaptive strategies to their habitat // Microsc. Res. Tech. 2021. V. 84. № 9. P. 1–15. https://doi.org/10.1002/jemt.23766
- Kattan G. H., Lillywhite H. B. Humidity acclimation and skin permeability in the lizard Anolis carolinensis // Physiol. Zool. 1989. V. 62. № 2. P. 593–606. https://doi.org/10.1086/physzool.62.2.30156187
- Landmann L. The sense organs in the skin of the head of Squamata (Reptilia) // Isr. J. Zool. 1975. V. 24. P. 99–135. https://doi.org/10.1080/00212210.1975.10688416
- Landmann L. Epidermis and dermis // Biology of Integument. V. 2. / Eds Bereiter-Hahn J., Matoltsy A. G., Richards K. S. Berlin, Heidelberg: Springer-Verlag, 1986. P. 150–187.
- Lillywhite H. B. Plasticity of the water barrier in vertebrate integument // International Congress Series. 2004. V. 1275. P. 283–290.
- Lillywhite H. B. Water relations of tetrapod integument // J. Exp. Biol. 2006. V. 209. № 2. P. 202–226. https://doi.org/10.1242/jeb.02007
- Maderson P. F. A. Keratinized epidermal derivatives as an aid to climbing in gekkonid lizards // Nature. 1964. V. 203. P. 780−781. https://doi.org/ 10.1038/203780a0
- Maderson P. F. A. The structure and development of the squamate epidermis // Biology of the skin and hair growth / Eds Lyne A. G., Short B. F. Sydney: Angus & Robertson, 1965. P.129–153.
- Maderson P. F. A. Lizard glands and lizard hands: models for evolutionary study // Forma et Functio. 1970. V. 3. P. 179−204.
- Maderson P. F. A. Some developmental problems of the reptilian integument // Biology of the Reptilia / Eds Hans C., Billett F., Maderson P. F.A. . 1985. V. 14. P. 525−598.
- Maderson P. F. A., Licht P. Epidermal morphology and sloughing frequency in normal and prolactin treated Anolis carolinensis (Iguanidae, Lacertilia) // J. Morphol. 1967. V. 123. P. 157–172. https://doi.org/10.1002/jmor.1051230205
- Mi Ch., Ma L., Wang Y., Wu D., Du W., Sun B. Temperate and tropical lizards are vulnerable to climate warming due to increased water loss and heat stress // Proc. Biol. Sci. 2022. V. 289. № 1980. P. 20221074. https://doi.org/10.1098/rspb.2022.1074
- Mittal A. K., Singh J. P. A. Hinge epidermis of Natrix piscator during its sloughing cycle – structural organization and protein histochemistry // J. Zool. 1987. V. 213. № 4. P. 685–695.
- Mohammed M. B. H. Skin development in the lizard embryo, Chalcides ocellatus forscae (Scincidae, Sauria, Reptilia) // Wasm. J. Biol. 1987. V. 45. № 1−2. P. 49−58.
- Roberts J. B., Lillywhite H. B. Lipid barrier to water exchange in Reptile epidermis // Science. 1980. V. 207. № 4435. P. 1077–1079. https://doi.org/10.1126/science.207.4435.1077
- Rutland C. S., Cigler P., Kubale V. Reptilian skin and its special histological structure // Veterinary Anatomy and Physiology / Eds Rutland C. S., Kubale V. IntechOpen. 2019. P. 1–21. www.intecho.com http://dx.doi.org/10.5772/intechopen.84212
- Sherbrooke W. C., Scardino A. J., Rocke de Nys, Schwarzkopf L. Functional morphology of hinges used to transport water: Convergent drinking adaptations in desert lizards (Moloch herridus and Phrynosoma cornutum) // Zoomorphology. 2007. V. 126. P. 89–102. https://doi.org/10.1007/s00435-007-0031-7
- Swadźba E., Rupik W. Ultrastructural studies of epidermis keratinization in grass snake embryos Natrix natrix L. (Lepidosauria, Serpentes) during late embryogenesis // Zoology. 2010. V. 113. P. 339–360. https://doi.org/10.1016/j.zool.2010.07.002
- Yenmiş M., Ayaz D., Sherbrooke W. C., Veselý M. A comparative behavioural and structural study of rain-harvesting and non-rain-harvesting agamid lizards of Anatolia (Turkey) // Zoomorphology. 2016. V. 135. № 1. P. 137–148. https://doi.org/10.1007/s00435-015-0285-4
- Žagar A., Vrezec A., Carretero M. A. Do the thermal and hydric physiologies of Zootoca (vivipara) carniolica (Squamata: Lacertidae) reflect the conditions of its selected microhabitat? // Salamandra. 2017. V. 53. № 1. P. 153–159.
Arquivos suplementares
