Article

Article name COUPLED VARIATION OF RED-BACKED VOLE SPECIES IN BIOTOPES DISTURBED BY WINDFALL AND FIRE IN THE VISIM STATE NATURE RESERVE (THE MIDDLE URALS)
Authors

Alexei G. Vasilyev, Dr. Sc., Professor, Head of Laboratory, Institute of Plant and Animal Ecology, Ural Branch of RAS (620144, Russia, Yekaterinburg, 8 March Street, 202); iD ORCID: https://orcid.org/0000-0002-5062-7288; e-mail: vag@ipae.uran.ru
Larisa E. Lukyanova, Dr. Sc., Leading Researcher, Institute of Plant and Animal Ecology, Ural Branch of RAS (620144, Russia, Yekaterinburg, 8 March Street, 202); iD ORCID: https://orcid.org/0000-0001-8665-1047; e-mail: lukyanova@ipae.uran.ru
Yulia V. Gorodilova, PhD, Senior Researcher, Institute of Plant and Animal Ecology, Ural Branch of RAS (620144, Russia, Yekaterinburg, 8 March Street, 202); iD ORCID: https://orcid.org/0000-0002-4358-3969; e-mail: gorodilova@ipae.uran.ru

Reference to article

Vasilyev A.G., Lukyanova L.Е., Gorodilova Yu.V. 2023. Coupled variation of red-backed vole species in biotopes disturbed by windfall and fire in the Visim State Nature Reserve (the Middle Urals). Nature Conservation Research 8(3): 24–46. https://dx.doi.org/10.24189/ncr.2023.020

Section Research articles
DOI https://dx.doi.org/10.24189/ncr.2023.020
Abstract

The use of morphogenetic characteristics and functionally important morphological structures in monitoring natural populations and communities is one of the modern directions in developing approaches to eco-morphology and functional synecology. New approaches make it possible to test the hypothesis of a similar spectrum of morphogenetic modifications of sympatric species during their development in disturbed biotopes. In this study, the coupled variability of the size and shape of the mandible was studied for the first time using geometric morphometrics to assess the resistance of the rodent community to two natural catastrophic phenomena (windfall and wildfire) for three sympatric red-backed vole species in the Visim State Nature Reserve (Middle Urals). Samples of Clethrionomys glareolus, Clethrionomys rutilus and Craseomys rufocanus young-of-the-years were studied in two biotopes modified by windfall and fire impacts under different weather conditions (2003 vs. 2004). It was found that Clethrionomys glareolus preferred the overgrown fire-damaged site, Craseomys rufocanus the windfall zone, and Clethrionomys rutilus did not express a pronounced preference. Interannual and biotopic differences in the variation of the size and shape of the mandible have been revealed for all species. Weather conditions affected the species variability more than biotopic ones. Based on functional mandibular indices, it was found that the shape of the mandible of the species, as a biological tool for foraging and its primary processing, depends more on weather factors than on the biotope characteristics. A similar morphofunctional reaction of sympatric species populations to similar biotopes was expressed. This fact reflects the parallelism of modifications of the morphogenesis of mandibles of the studied species in disturbed biotopes, confirming the hypothesis. In particular, in the fire-damaged site, the tendency to longitudinal grinding of feed was revealed for all species, while in the windfall zone, the tendency to gnawing of forage objects (possibly, seeds of coniferous plants) was revealed. It is assumed that weather factors indirectly affect the morphogenesis of species through the change of plant communities, which, in turn, changes the diet of animals and the mechanics of the load on the musculoskeletal apparatus of mandibles. The within-group morphological disparity (MNND), which reflects the measure of destabilisation of development, was small in Clethrionomys glareolus, indicating the stability of its morphogenesis in both biotopes; the development of Craseomys rufocanus was stable only on the windfall site; in Clethrionomys rutilus, MNND was unstable in both biotopes. The MNND development stability estimates are consistent with the species abundance. They are recommended for monitoring the population status of sympatric species of the red-backed voles and other rodents in Protected Areas.

Keywords

development stability, geometric morphometrics, mandible, natural catastrophe, Protected Area, rodents, variation

Artice information

Received: 07.02.2023. Revised: 12.04.2023. Accepted: 19.04.2023.

The full text of the article
References

Abramson N.I., Petrova T.P., Dokuchaev N.E., Obolenskaya E.A., Lissovsky A.A. 2012. Phylogeography of the gray red-backed vole Craseomys rufocanus (Rodentia: Cricetidae) across the distribution range inferred from nonrecombining molecular markers. Russian Journal of Theriology. Vol. 11(2): 137–156. DOI: 10.15298/rusjtheriol.11.2.04
Ackerly D.D., Cornwell W.K. 2007. A trait-based approach to community assembly: partitioning of species trait values into within- and among-community components. Ecology Letters 10(2): 135–145. DOI: 10.1111/j.1461-0248.2006.01006.x
Anderson P.S.L., Renaud S., Rayfield E.J. 2014. Adaptive plasticity in the mouse mandible. BMC Evolutionary Biology 14: 85. DOI: 10.1186/1471-2148-14-85
Andrews P., Hixson S. 2014. Taxon-free methods of palaeoecology. Annales Zoologici Fennici 51(1–2): 269–284. DOI: 10.5735/086.051.0225
Artsybashev E.S. 2014. The impact of forest fires on silvan biogeocenoses. Biosfera 6(1): 53–59. DOI: 10.24855/biosfera.v6i1.204 [In Russian]
Badyaev A.V. 2014. Epigenetic resolution of the 'curse of complexity' in adaptive evolution of complex traits. Journal of Physiology 592(11): 2251–2260. DOI: 10.1113/jphysiol.2014.272625
Badyaev A.V., Foresman K.R., Young R.L. 2005. Evolution of Morphological Integration: Developmental Accommodation of Stress‐Induced Variation. American Naturalist. Vol. 166(3): 382–395. DOI: 10.1086/432559
Barnosky A.D., Matzke N., Tomiya S., Wogan G.O.U., Swartz B., Quental T.B., Marshall C., McGuire J.L., Lindsey E.L., Maguire K.C., Mersey B., Ferrer E.A. 2011. Has the Earth's sixth mass extinction already arrived?. Nature 471(7336): 51–57. DOI: 10.1038/nature09678
Bashenina N.V. 1977. Ways of adaptations of mouse-like rodents. Moscow: Nauka. 354 p. [In Russian]
Berdyugin K.I. 1999. Rodent communities of the Northern Urals. Russian Journal of Ecology 30(2): 119–125.
Bolshakova N.P. 2010. Ecological-physiological and ethological characteristics of populations of forest voles (Clethrionomys) in co-habitation. PhD Thesis Abstract. Tomsk. 22 p. [In Russian]
Bond D.P.G., Grasby S.E. 2017. On the causes of mass extinctions. Palaeogeography, Palaeoclimatology, Palaeoecology 478: 3–29. DOI: 10.1016/j.palaeo.2016.11.005
Carleton M.D., Gardner A.L., Pavlinov I.Ya., Musser G.G. 2014. The valid generic name for red-backed voles (Muroidea: Cricetidae: Arvicolinae): restatement of the case for Myodes Pallas, 1811. Journal of Mammalogy 95(5): 943–959. DOI: 10.1644/14-MAMM-A-004
Ceballos G., Ehrlich P.R., Barnosky A.D., García A., Pringle R.M., Palmer T.M. 2015. Accelerated modern human-induced species losses: entering the sixth mass extinction. Science Advances. Vol. 1(5): e1400253. DOI: 10.1126/sciadv.1400253
Chernov Yu.I. 2008. Ecology and biogeography. Selected paper. Moscow: KMK Scientific Press Ltd. 580 p. [In Russian]
Chevin L.M., Lande R., Mace G.M. 2010. Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLoS Biology 8(4): e1000357. DOI: 10.1371/journal.pbio.1000357
Cohen J. 1992. A power primer. Psychology Bulletin 112(1): 155–159. DOI: 10.1037//0033-2909.112.1.155
Cornette R., Tresset A., Herrel A. 2015. The shrew tamed by Wolff's Law: Do functional constraints shape the skull through muscle and bone covariation?. Journal of Morphology 276(3): 301–309. DOI: 10.1002/jmor.20339
Cornwell W.K., Schwilk D.W., Ackerly D.D. 2006. A trait-based test for habitat filtering: Convex hull volume. Ecology 87(6): 1465–1471. DOI: 10.1890/0012-9658(2006)87[1465:attfhf]2.0.co;2
Damuth J.D., Jablonski D., Harris R.M., Potts R., Stucky R.K., Sues H.D., Weishampel D.B. 1992. Taxon-free characterization of animal communities. In: A.K. Beherensmeyer, J.D. Damuth, W.A. Di Michele, R. Potts, H.D. Sues., S.L. Wing (Eds.): Terrestrial Ecosystems Through Time: Evolutionary Paleoecology of Terrestrial Plants and Animals. Chicago, USA: University of Chicago Press. P. 183–203.
Davis D.S. 1990. Statistical analysis data in geology. Book 2. Moscow: Nedra. 427 p. [In Russian]
Donelan S.C., Hellmann J.K., Bell A.M., Luttbeg B., Luttbeg J.C., Orrock J.L., Sheriff M.J., Sih A. 2020. Transgenerational plasticity in human-altered environments. Trends in Ecology and Evolution 35(2): 115–124. DOI: 10.1016/j.tree.2019.09.003
Donnelly K.P. 1978. Simulations to determine the variance and edge effect of total nearest neighbor distance. In: I. Hodder (Ed.): Simulation studies to archeology. Cambridge: Cambridge University Press. P. 91–95.
Fontaneto D., Panisi M., Mandrioli M., Montardi D., Pavesi M., Cardini A. 2017. Estimating the magnitude of morphoscapes: how to measure the morphological component of biodiversity in relation to habitats using geometric morphometrics. Science of Nature 104(7–8): 55. DOI: 10.1007/s00114-017-1475-3
Gongalsky K.B. 2014. Forest fires and soil fauna. Moscow: KMK Scientific Press Ltd. 169 p. [In Russian]
Gromov I.M., Erbaeva M.A. 1995. Mammals of the fauna of Russia and adjacent territories. Lagomorpha and Rodents. St. Petersburg: Zoological Institute RAS. 522 p. [In Russian]
Hammer Ø. 2009. New statistical methods for detecting point alignments. Computers and Geosciences 35(3): 659–666. DOI: 10.1016/j.cageo.2008.03.012
Hammer Ø., Harper D.A.T., Ryan P.D. 2001. PAST: Paleontological Statistics software package for education and data analysis. Palaeontologia Electronica 4(1): 1–9.
Hanski I. 1998. Metapopulation dynamics. Nature 396(6706): 41–49. DOI: 10.1038/23876
Hedges L.V., Olkin I. 1985. Statistical methods for Meta-Analysis. New York: Academic Press. 369 p.
Hutchinson G.E. 1967. Treatise on Limnology. Vol. 2. Introduction to Lake Biology and the Limnoplankton. New York: John Wiley & Sons. 1115 p.
Jones K., Law C.J. 2018. Differentiation of craniomandibular morphology in two sympatric Peromyscus mice (Cricetidae: Rodentia). Mammal Research 63(3): 277–283. DOI: 10.1007/s13364-018-0364-2
Kaneko Y., Nakata K., Saitoh T., Stenseth N.C., Bjørnstad O.N. 1998. The biology of the vole Clethrionomys rufocanus: a review. Population Ecology 40(1): 21–37. DOI: 10.1007/BF02765219
Kharitonova A.O., Kharitonova T.I. 2021. The effect of landscape pattern on the 2010 wildfire spread in the Mordovia State Nature Reserve, Russia. Nature Conservation Research 6(2): 29–41. DOI: 10.24189/ncr.2021.022 [In Russian]
Klingenberg C.P. 2011. MorphoJ: an integrated software package for geometric morphometrics. Molecular Ecology Resources 11(2): 353–357. DOI: 10.1111/j.1755-0998.2010.02924.x
Kravchenko L.B. 1999. Community dynamics and population features of forest voles (Clethrionomys) of the Middle Ob floodplain. PhD Thesis Abstract. Tomsk. 22 p. [In Russian]
Kruskal J.B. 1964a. Multidimensional scaling by optimizing goodness of fit to a nonmetric hypothesis. Psychometrika 29: 1–27. DOI: 10.1007/BF02289565
Kruskal J.B. 1964b. Nonmetric multidimensional scaling: a numerical method. Psychometrika 29: 115–129. DOI: 10.1007/BF02289694
Kryštufek B., Tesakov A.S., Lebedev V.S., Bannikova A.A., Abramson N.I., Shenbrot G. 2020. Back to the future: The proper name for red-backed voles is Clethrionomys Tilesius and not Myodes Pallas. Mammalia 84(2): 214–217. DOI: 10.1515/mammalia-2019-0067
Lebedev V.S., Bannikova A.A., Tesakov A.S., Abramson N.I. 2007. Molecular phylogeny of the genus Alticola (Cricetidae, Rodentia) as inferred from the sequence of the cytochrome b gene. Zoologica Scripta 36(6): 547–563. DOI: 10.1111/j.1463-6409.2007.00300.x
Lukyanova L.E. 2013. Association of sympatric small mammal species under contrasting environmental conditions. Russian Journal of Ecology 44(1): 60–67. DOI: 10.1134/S1067413613010098
Lukyanova L.E. 2017. Effect of ecotone at the boundary of windfall- and fire-damaged forest biocenoses on the abundance of rodents and characteristics of their microhabitats. Russian Journal of Ecology 48(3): 245–250. DOI: 10.1134/S1067413617030092
Maestri R., Monteiro L.R., Fornel R., de Freitas T.R.O., Patterson B.D. 2018. Geometric morphometrics meets metacommunity ecology: environment and lineage distribution affects spatial variation in shape. Ecography 41(1): 90–100. DOI: 10.1111/ecog.03001
Mo J., Polly P.D. 2022. The role of dispersal, selection intensity, and extirpation risk in resilience to climate change: A trait-based modelling approach. Global Ecology and Biogeography 31(6): 1184–1193. DOI: 10.1111/geb.13495
Nikolaev I.I. 1977. Taxocene as an ecological category. Ecologiya 5: 50–55. [In Russian]
Ognev S.I. 1950. Mammals of the USSR and adjacent countries. Vol. 7. Moscow-Leningrad: Publishing House of AS USSR. 715 p. [In Russian]
Parmesan C. 2006. Ecological and evolutionary responses to recent climate change. Annual Review of Ecology, Evolution, and Systematics 37: 637–669. DOI: 10.1146/annurev.ecolsys.37.091305.110100
Pausas J.G., Verdú M. 2008. Fire reduces morphospace occupation in plant communities. Ecology 89(8): 2181–2186. DOI: 10.1890/07-1737.1
Pavlinov I.Ya. 2006. Systematics of Recent Mammals. Archive of Zoological Museum of Moscow State University 47: 1–287.
Potapova E.G. 2019. Morphofunctional transformation of chew gnathic musculature in evolution of rodents. Zhurnal Obshchei Biologii 80(4): 260–273. DOI: 10.1134/S0044459619040079 [In Russian]
Read A.F., Clark J.S. 2006. The next 20 years of ecology and evolution. Trends in Ecology and Evolution 21(7): 354–355. DOI: 10.1016/j.tree.2006.05.003
Ricotta C., Moretti M. 2011. CWM and Rao's quadratic diversity: a unified framework for functional ecology. Oecologia 167(1): 181–188. DOI: 10.1007/s00442-011-1965-5
Rohlf F.J. 2013a. TPSUtility Program, version 1.56. Stony Brook, NY: Department of Ecology and Evolution, State University of New York.
Rohlf F.J. 2013b. TPSDig, version 2.17. Stony Brook, NY: Department of Ecology and Evolution, State University of New York.
Rohlf F.J., Slice D. 1990. Extensions of the Procrustes Method for the Optimal Superimposition of Landmarks. Systematic Biology 39(1): 40–59. DOI: 10.2307/2992207
Schleuning M., Neuschulz E.L., Albrecht J., Bender I.M.A., Bowler D.E., Dehling D.M., Fritz S.A., Hof C., Mueller T., Nowak L., Sorensen M.C., Böhning-Gaese K., Kissling W.D. 2020. Trait-based assessments of climate-change impacts on interacting species. Trends in Ecology and Evolution 35(4): 319–328. DOI: 10.1016/j.tree.2019.12.010
Sheets H.D., Zelditch M.L. 2013. Studying ontogenetic trajectories using resampling methods and landmark data. Hystrix 24(1): 67–73. DOI: 10.4404/hystrix-24.1-6332
Schmalhausen I.I. 1968. Factors of evolution. Moscow: Nauka. 451 p. [In Russian]
Shvarts S.S. 1977. The evolutionary ecology of animals. Ecological mechanisms of the evolutionary process. New York: Consultants Bureau. 292 p.
Sokolov V.E. (Ed.). 1981. European red vole. Moscow: Nauka. 352 p. [In Russian]
StatSoft, Inc. 2011. Electronic statistics textbook. Tulsa, USA: StatSoft. Available from https://www.statsoft.com/textbook
Taguchi Y.H., Oono Y. 2005. Relational patterns of gene expression via non-metric multidimensional scaling analysis. Bioinformatics 21(6): 730–740. DOI: 10.1093/bioinformatics/bti067
Tesakov A.S., Lebedev V.S., Bannikova A.A., Abramson N.I. 2010. Clethrionomys Tilesius, 1850 is the valid generic name for red-backed voles and Myodes Pallas, 1811 is a junior synonym of Lemmus Link, 1795. Russian Journal of Theriology 9(2): 83–86. DOI: 10.15298/rusjtheriol.09.2.04
Vasil'ev A.G. 2021. The Concept of Morphoniche in Evolutionary Ecology. Russian Journal of Ecology 52(3): 173–187. DOI: 10.1134/S1067413621030097
Vasil'ev A.G., Vasil'eva I.A., Kourova T.P. 2015. Analysis of coupled geographic variation of three shrew species from southern and northern Ural taxocenes. Russian Journal of Ecology 46(6): 552–558. DOI: 10.1134/S1067413615060223
Vasil'ev A.G., Bol'shakov V.N., Vasil'eva I.A., Evdokimov N.G., Sineva N.V. 2016. Assessment of nonselective elimination effects in rodent communities by methods of geometric morphometrics. Russian Journal of Ecology 47(4): 383–391. DOI: 10.1134/S1067413616040159
Vasil'ev A.G., Vasil'eva I.A., Gorodilova Yu.V., Dobrinskii N.L. 2017. Chernov's compensation principle and the effect of rodent community completeness on the variability of Bank vole (Clethrionomys glareolus) population in the Middle Urals. Russian Journal of Ecology 48(2): 161–169. DOI: 10.1134/S106741361702009
Vasilyev A.G., Vasilyeva I.A., Shkurikhin A.O. 2018. Geometric morphometrics: from theory to practice. Moscow: KMK Scientific Press Ltd. 471 p. [In Russian]
Vasil'ev A.G., Bol'shakov V.N., Vasil'eva I.A. 2020. Intra- and interpopulation odontological variability in the Gray Red-backed Vole (Craseomys rufocanus) and Yu.I. Chernov's Compensation Principle. Russian Journal of Ecology 51(1): 1–10. DOI: 10.1134/S1067413620010130
Vasil'ev A.G., Lukyanova L.E., Gorodilova Yu.V. 2022. The ratio of biotopic and interannual variability of bank voles in windfall- and fire-transformed forest biotopes of the Middle Urals. Russian Journal of Ecology 53(6): 515–527. DOI: 10.1134/S1067413622060170
Violle C., Enquist B.J., McGill B.J., Jiang L., Albert C.H., Hulshof C., Jung V., Messier J. 2012. The return of the variance: intraspecific variability in community ecology. Trends in Ecology and Evolution 27(4): 244–252. DOI: 10.1016/j.tree.2011.11.014
Vorontsov N.N. 1982. The lower Cricetidae of the world fauna, Part 1. Morphology and ecology. The Fauna of the Soviet Union. Mammals. Vol. 3. Leningrad: Nauka. 451 p. [In Russian]
Yamborko A.V. 2015. Population ecology of forest voles (genus Clethrionomys) in Northeast Asia. PhD Thesis Abstract. Vladivostok. 24 p. [In Russian]
Young R.L., Sweeney M.J., Badyaev A.V. 2010. Morphological diversity and ecological similarity: versatility of muscular and skeletal morphologies enables ecological convergence in shrews. Functional Ecology 24(3): 556–565. DOI: 10.1111/j.1365-2435.2009.01664.x
Zakharov V.M. 1992. Population phenogenetics: Analysis of developmental stability in natural populations. Acta Zoologica Fennica 191: 7–30.
Zelditch M.L., Swiderski D.L., Sheets H.D., Fink W.L. 2004. Geometric Morphometrics for Biologists. A Primer. New York: Academic Press. 437 p. DOI: 10.1016/B978-0-12-778460-1.X5000-5
Zherikhin V.V. 2003. Selected papers on palaeoecology and phylocoenogenetics. Moscow: KMK Scientific Press Ltd. 542 p. [In Russian]