Abstract
Changing environmental conditions in the Arctic make it important to document and understand habitat preferences and flexibility of vulnerable high-latitude mammals. Indirect proxies are especially useful for elusive species, such as rodents. This study explores incisor microwear as an indicator of variation in behavior and microhabitat use in Siberian lemmings (Lemmus sibiricus) and narrow-headed voles (Lasiopodomys gregalis) from the Yamal Peninsula, Russia. Fifty-nine individuals were sampled at four sites along a latitudinal gradient from forest-tundra ecotone to high-Arctic tundra. Lemmings are present at the northernmost site, voles at the southernmost site, and both species at the middle two. Lemmus sibiricus prefers wet, mossy lowland, whereas La. gregalis favors drier thickets and more open microhabitats and burrows underground. Feature-based analyses indicate higher densities of features and more uniformly oriented striations for voles than lemmings at sites with both species. The species also differ significantly in microwear texture attributes suggesting larger features for lemmings, and smaller ones, but more of them, for voles. While no texture differences were found between sites within species, voles from sites with open tundra have higher striation densities than those from the forest-tundra ecotone. Furthermore, lemmings from open tundra sites have higher striation densities than those from the water-saturated, moss-covered northernmost site. While microhabitat preferences and burrowing by voles likely contribute to differences between species, variation within seems to reflect habitat variation given differences in abrasive loads between sites. This suggests that incisor microwear patterning can be used to track microhabitat differences among Arctic rodent populations.
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Data availability
All raw data presented in this study are presented in Supplementary Information file (SI) 1. Original specimens are part of the permanent collection of the Institute of Plant and Animal Ecology in Labytnangi, Russia but currently on loan to the University of Burgundy, France.
References
Adams NF, Gray T, Purnell MA (2020) Dietary signals in dental microwear of predatory small mammals appear unaffected by extremes in environmental abrasive load. Palaeogeogr Palaeoclimatol Palaeoecol 558:109929
Alfredsson H, Clymans W, Hugelius G, Kuhry P, Conley DJ (2016) Estimated storage of amorphous silica in soils of the circum—Arctic tundra region. Glob Biogeochem Cycle 30:479–500
Arman SD, Ungar PS, Brown CA, DeSantis LRG, Schmidt C, Prideaux GJ (2016) Minimizing inter-microscope variability in dental microwear texture analysis. Surf Topogr Metrol 4:024007
Baca M, Popovic D, Lemanik A, Baca K, Horacek I, Nadachowski A (2019) Highly divergent lineage of narrow-headed vole from the Late Pleistocene Europe. Sci Rep 9:17799
Baltensperger AP, Huettmann F, Hagelin JC, Welker JM (2015) Quantifying trophic niche spaces of small mammals using stable isotopes (δ15N and δ13C) at two scales across Alaska. Can J Zool 93:579–588
Bashenina N (1962) Ecology of common vole with some features of its geographical variability (In Russian). Moscow University Press, Moscow
Batsaikhan N, Tsytsulina K, Formozov N, Sheftel B (2016) Microtus gregalis. The IUCN red list of threatened species e-T13431A1.
Belmaker M (2018) Dental microwear of small mammals as a high resolution paleohabitat proxy: opportunities and challenges. J Archaeol Sci Rep 18:824–838
Belmaker M, Ungar PS (2010) Micromammal microwear texture analysis—preliminary results and applications for paleoecological study. Abstr Paleoanthropology Soc 2:A2
Budaev SV (2010) Using principal components and factor analysis in animal behaviour research: caveats and guidelines. Ethology 116:472–480
Burgman JHE, Leichliter J, Avenant NL, Ungar PS (2016) Dental microwear of sympatric rodent species sampled across habitats in southern Africa: implications for environmental influence. Integr Zool 11:111–127
Calandra I, Merceron G (2016) Dental microwear texture analysis in mammalian ecology. Mamm Rev 46:215–228
Calandra I, Labonne G, Mathieu O, Henttonen H, Leveque J, Milloux MJ, Renvoise E, Montuire S, Navarro N (2015) Isotopic partitioning by small mammals in the subnivium. Ecol Evol 5:4132–4140
Calandra I, Labonne G, Schulz-Kornas E, Kaiser TM, Montuire S (2016) Tooth wear as a means to quantify intra-specific variations in diet and chewing movements. Sci Rep 6:34037
Caporale SS, Ungar PS (2016) Rodent incisor microwear as a proxy for ecological reconstruction. Palaeogeogr Palaeoclimatol Palaeoecol 446:225–233
Carey JC, Fulweiler RW (2012) The terrestrial silica pump. PLoS ONE 7:e52932
CAVM Team (2003) Circumpolar Arctic Vegetation Map, scale 1:7 500 000. Conservation of Arctic Flora and Fauna (CAFF) Map No. 1. US Fish and Wildlife Service, Anchorage, AK.
Cerny BA, Kaiser HF (1977) A study of a measure of sampling adequacy for factor-analytic correlation matrices. Multivar Behav Res 12:43–47
Chajewski M (2009) Rela: scale item analysis. R Package. version 4
Christensen TR, Payne J, Doyle G, Ibarguchi G, Taylor NM, Schmidt M, Gill M, Svoboda M (2013) The Arctic terrestrial biodiversity monitoring plan. CAFF International Secretariat, Akureyri
Coady JM, Toto PD, Santangelo MV (1967) Histology of the mouse incisor. J Dent Res 46:384–388
Conover WJ, Iman RL (1981) Rank transformations as a bridge between parametric and nonparametric statistics. Am Stat 35:124–129
Cook RJ, Farewell VT (1996) Multiplicity considerations in the design and analysis of clinical trials. J R Stat Soc Ser A 159:93–110
DeSantis LRG (2016) Dental microwear textures: reconstructing diets of fossil mammals. Surf Top Met Prop 4:023002
Dunaeva TN (1948) Comparative ecology of the tundra voles of Yamal Peninsula (In Russian). Proc Inst Geogr USSR Acad Sci 41:78–143
Ehrich D, Schmidt NM, Gauthier G, Alisauskas R, Angerbjorn A, Clark K, Ecke F, Eide NE, Framstad E, Frandsen J, Franke A, Gilg O, Goiroux M-A, Henttonen H, Bierger H, Ims RA, Kataev GD, Kharitonov SP, Krebs CJ, Killengreen ST, Lanctot RB, Lecomte N, Menyushina IR, Morris DW, Morrisson G, Oksanen L, Oksanen T, Olofsson J, Pokrovsky IG, Popov IY, Reid D, Roth JD, Samelius G, Sittler B, Sleptsov SM, Smith P, Sokolov AA, Sokolova NA, Soloviev MY, Solovyeva D (2020) Documenting lemming population change in the Arctic: can we detect trends? Ambio 49:786–800
Firmat C, Rodrigues HG, Renaud S, Claude J, Hutterer R, Garcia-Talavera F, Michaux J (2010) Mandible morphology, dental microwear, and diet of the extinct giant rats Canariomys (Rodentia: Murinae) of the Canary Islands (Spain). Biol J Linn Soc 101:28–40
Firmat C, Rodrigues HG, Hutterer R, Rando JC, Alcover JA, Michaux J (2011) Diet of the extinct Lava mouse Malpaisomys insularis from the Canary Islands: insights from dental microwear. Naturwissenschaften 98:33–37
Gilg O, Sittler B, Hanski I (2009) Climate change and cyclic predator-prey population dynamics in the high Arctic. Glob Change Biol 15:2634–2652
Grine FE (1986) Dental evidence for dietary differences in Australopithecus and Paranthropus: a quantitative analysis of permanent molar microwear. J Hum Evol 15:783–822
Grine FE, Ungar PS, Teaford MF (2002) Error rates in dental microwear quantification using scanning electron microscopy. Scanning 24:144–153
Gromov IM, Polyakov IY (1992) Voles (Microtinae). Fauna of the USSR mammals, vol III. E.J. Brill, Leiden
Hautier L, Bover P, Alcover JA, Michaux J (2009) Mandible morphometrics, dental microwear pattern, and palaeobiology of the extinct Balearic Dormouse Hypnomys morpheus. Acta Palaeontol Pol 54:181–194
Hua LC, Brandt ET, Meullenet JF, Zhou ZR, Ungar PS (2015) Technical note: an in vitro study of dental microwear formation using the BITE Master II chewing machine. Am J Phys Anthropol 158:769–775
Ims RA, Yoccoz NG, Killengreen ST (2011) Determinants of lemming outbreaks. Proc Natl Acad Sci US 108:1970–1974
Kalthoff DC, Schulz-Kornas E, Corfe I, Martin T, McLoughlin S, Schultz JA (2019) Complementary approaches to tooth wear analysis in Tritylodontidae (Synapsida, Mammaliamorpha) reveal a generalist diet. PLoS ONE 14:e0220199
Kausrud KL, Mysterud A, Steen H, Vik JO, Ostbye E, Cazelles B, Framstad E, Eikeset AM, Mysterud I, Solhoy T, Stenseth NC (2008) Linking climate change to lemming cycles. Nature 456:93-97
Klevezal GA (2010) Dynamics of incisor growth and daily increments on the incisor surface in three species of small rodents. Biol Bull 37:836–845
Klevezal GA, Pucek M, Sukhovskaja LI (1990) Incisor growth in voles. Acta Ther 35:331–344
Kopein KI (1958) Materials on the biology of the Siberian lemming and the narrow-headed vole (In Russian). Bull MOIP Ural Dept 1:109–133
Kropacheva YE, Sibiryakov PA, Smirnov NG, Zykov SV (2017) Variants of tooth mesowear in Microtus voles as indicators of food hardness and abrasiveness. Russ J Ecol 48:73–80
Magomedova MA, Morozova LM, Ektova SN, Rebristaya OV, Chernyadeva IV, Potemkin AD, Knyazev MC (2006) Yamal Peninsula: vegetation cover. City Press, Tyumen
Markova AK, van Kolfschoten T, Bohncke S, Kosintsev PA, Mol J, Yu A, Puzachenko AN, Simakova AN, Smirnov NG, Verpoorte A, Golovachev IB (2019) Evolution of the European ecosystems during Pleistocene-Holocene transition (24–8 kyr BP). GEOS Press, Moscow
Martin LF, Krause L, Ulbricht A, Winkler DE, Codron D, Kaiser TM, Muller J, Hummel J, Clauss M, Hatt JM, Schulz-Kornas E (2020) Dental wear at macro- and microscopic scale in rabbits fed diets of different abrasiveness: a pilot investigation. Palaeogeogr Palaeoclimatol Palaeoecol 556:109886
Melnikov YS (1991) Commentaries to the map of natural complexes (In Russian). VSEGINGEO Press, Moscow
Merceron G, Blondel C, Brunetiere N, Francisco A, Gautier D, Ramdarshan A (2017) Dental microwear and controlled food testing on sheep: the TRIDENT project. Biosurf Biotribol 3:174–183
Myllymäki A, Paasikallio A, Pankakoski E, Kanervo V (1971) Removal experiments on small quadrats as a mean of rapid assessment of the abundance of small mammals. Ann Zool Fenn 8:177–185
Nelson S, Badgley C, Zakem E (2005) Microwear in modern squirrels in relations to diet. Palaeontol Electron 8:1–15
Pal’chekh NA, Mal’kova MG, Kuz’min IV, Yakimenko VV (2003) The structure of narrow-skulled vole (Microtus gregalis Pall.) colonies in western Siberia. Russ J Ecol 34:327–331
Perneger TV (1998) What’s wrong with Bonferroni adjustments. Br Med J 316:1236–1238
Post E, Forchhammer MC, Bret-Harte MS, Callaghan TV, Christensen TR, Elberling B, Fox AD, Gilg O, Hik DS, Hoye TT, Ims RA, Jeppesen E, Klein DR, Madsen J, McGuire AD, Rysgaard S, Schindler DE, Stirling I, Tamstorf MP, Tyler NJC, van der Wal R, Welker J, Wookey PA, Schmidt NM, Aastrup P (2009) Ecological dynamics across the Arctic associated with recent climate change. Science 325:1355–1358
Purnell MA, Crumpton N, Gill PG, Jones G, Rayfield EJ (2013) Within-guild dietary discrimination from 3-D textural analysis of tooth microwear in insectivorous mammals. J Zool 291:249–257
R Core Team (2021) R: a language and environment for statistical computing. Version 4.0.5. R Foundation for Statistical Computing, Vienna
Robinet C, Merceron G, Candela AM, Marivaux L (2020) Dental microwear texture analysis and diet in caviomorphs (Rodentia) from the Serra do Mar Atlantic forest (Brazil). J Mamm 101:386–402
Rodrigues HG, Merceron G, Viriot L (2009) Dental microwear patterns of extant and extinct Muridae (Rodentia, Mammalia): ecological implications. Naturwissenschaften 96:537–542
Rodrigues HG, Renaud S, Charles C, Le Poul Y, Sole F, Aguilar JP, Michaux J, Tafforeau P, Headon D, Jernvall J, Viriot L (2013) Roles of dental development and adaptation in rodent evolution. Nat Comm 4:2504
Schmidt NM, Ims RA, Hoye TT, Gilg O, Hansen LH, Hansen J, Lund M, Fuglei E, Forchhammer MC, Sittler B (2012) Response of an arctic predator guild to collapsing lemming cycles. Proc Biol Sci 279:4417–4422
Schulz E, Calandra I, Kaiser TM (2010) Applying tribology to teeth of hoofed mammals. Scanning 32:162–182
Schulz E, Piotrowski V, Clauss M, Mau M, Merceron G, Kaiser TM (2013) Dietary abrasiveness is associated with variability of microwear and dental surface texture in rabbits. PLoS ONE 8:e56167
Scott RS, Ungar PS, Bergstrom TS, Brown CA, Childs BE, Teaford MF, Walker A (2006) Dental microwear texture analysis: technical considerations. J Hum Evol 51:339–349
Soininen EM, Zinger L, Gielly L, Bellemain E, Brathen KA, Brochmann C, Epp LS, Gussarova G, Hassel K, Henden JA, Killengreen ST, Rama T, Stenoien HK, Yoccoz NG, Ims RA (2013) Shedding new light on the diet of Norwegian lemmings: DNA metabarcoding of stomach content. Polar Biol 36:1069–1076
Soininen EM, Ehrich D, Lecomte N, Yoccoz NG, Tarroux A, Berteaux D, Gauthier G, Gielly L, Brochmann C, Gussarova G, Ims RA (2014) Sources of variation in small rodent trophic niche: new insights from DNA metabarcoding and stable isotope analysis. Isot Environ Health Stud 50:361–381
Sokolova NA, Sokolov AA, Ims RA, Skogstad G, Lecomte N, Sokolov VA, Yoccoz NG, Ehrich D (2014) Small rodents in the shrub tundra of Yamal (Russia): density dependence in habitat use? Mamm Biol 79:306–312
Stuhlträger J, Schulz-Kornas E, Wittig RM, Kupczik K (2019) Ontogenetic dietary shifts and microscopic tooth wear in western chimpanzees. Front Ecol Evol 7:298
Teaford MF (1988) Scanning electron microscope diagnosis of wear patterns versus artifacts on fossil teeth. Scanning Microsc 2:1167–1175
Teaford MF, Oyen OJ (1989) In vivo and in vitro turnover in dental microwear. Am J Phys Anthropol 80:447–460
Teaford MF, Ungar PS, Taylor AB, Ross CF, Vinyard CJ (2020) The dental microwear of hard-object feeding in laboratory Sapajus apella and its implications for dental microwear formation. Am J Phys Anthropol 171:439–455
Townsend KEB, Croft DA (2008) Enamel microwear in caviomorph rodents. J Mamm 89:730–743
Trofimov VT (1986) Exogeodynamics of the West Siberian plate: spatio-temporal regularities (In Russian). Moscow State University Press, Moscow
Trofimov VT, Badu YB, Dubikov GI (1980) Cryogen structure and ice content of permafrost formations of the west siberian plate (In Russian). Moscow State University Press, Moscow
Tsytsulina K, Formozov N, Sheftel B (2016) Lemmus sibiricus. The IUCN Red List of Threatened Species e-T11482A3283480
Ungar PS (1994) Incisor microwear of Sumatran anthropoid primates. Am J Phys Anthropol 94:339–363
Ungar PS (1995) A semiautomated image analysis procedure for the quantification of dental microwear II. Scanning 7:57–59
Ungar PS (2002) Microware software: a semi-automated image analysis system for the quantification of dental microwear. Ed, 4.02 Unpublished, Fayetteville, AR
Ungar PS (2015) Mammalian dental function and wear: a review. Biosurf Biotribol 1:25–41
Ungar PS (2018) Tooth surface topography: a scale-sensitive approach with implications for inferring dental adaptation and diet. In: Anemone R, Conroy G (eds) New geospatial approaches in anthropology. SAR Press, Santa Fe, pp 101–120
Ungar PS, Simon JC, Cooper JW (1991) A semiautomated image-analysis procedure for the quantification of dental microwear. Scanning 13:31–36
Ungar PS, Brown CA, Bergstrom TS, Walkers A (2003) Quantification of dental microwear by tandem scanning confocal microscopy and scale-sensitive fractal analyses. Scanning 25:185–193
Ungar PS, Sokolova NA, Purifoy J, Fufachev IA, Sokolov AA (2021) Assessing molar wear in narrow-headed voles as a proxy for diet and habitat in a changing Arctic. Mamm Biol 101:137–151
Walker DA, Raynolds MK, Daniels FJA, Einarsson E, Arve E, Gould WA, Kaitenin AE, Kholod SS, Markon CJ, Melnikov ES, Moskalenko NG, Talbot SS, Yurtsev BA (2005) The circumolar arctic vegetation map. J Veg Sci 16:267–282
Winkler DE, Andrianasolo TH, Andriamandimbiarisoa L, Ganzhorn JU, Rakotondranary SJ, Kaiser TM, Schulz-Kornas E (2016) Tooth wear patterns in black rats (Rattus rattus) of Madagascar differ more in relation to human impact than to differences in natural habitats. Ecol Evol 6:2205–2215
Acknowledgements
We acknowledge the Russian Foundation for Basic Research, the Russian Center of Development of the Arctic, “Yamal-LNG” company and Government of the Yamal Nenets Autonomous District, and the University of Arkansas Honors College, for funds that allowed this work. The collaboration that led to this work was developed through support from the US National Science Foundation. We thank Miriam Belmaker for discussions related to this paper and Daniela Kalthoff and an anonymous reviewer for helpful comments on an earlier version of this paper.
Funding
NAS and AAS were supported through grant of Russian Foundation for Basic Research No: 18-05-60261, by the Russian Center of Development of the Arctic, “Yamal-LNG” company and Government of the Yamal Nenets Autonomous District. PSU and LS were funded by the University of Arkansas Honors College, and the collaboration that led to this work was developed through support from US National Science Foundation Award No: 1927793.
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PSU, OG, AAS, NAS, SM, and AR conceived of the project, analyzed the data and wrote the paper. NAS, IF, and AAS collected original specimens analyzed in this paper. LS generated the digital models and photosimulations of the microwear surfaces, and PSU took the dental impressions and generated the microwear data.
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Ungar, P.S., Saylor, L., Sokolov, A.A. et al. Incisor microwear of Arctic rodents as a proxy for microhabitat preference. Mamm Biol 101, 1033–1052 (2021). https://doi.org/10.1007/s42991-021-00138-x
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DOI: https://doi.org/10.1007/s42991-021-00138-x