Abstract
Studies of the effects of variation in resource availability are important for understanding the ecology of high-latitude mammals. This paper examines the potential of dental evidence (tooth wear and breakage) as a proxy for diet and food choice in Vulpes lagopus, the Arctic fox. It presents a preliminary study of dental microwear, gross wear score, and tooth breakage in a sample (n = 78 individuals) from the Yamal Peninsula of the Russian Arctic. While these measures have each been associated with feeding ecology in larger carnivorans (e.g., proportion of bone in the diet), they have yet to be combined in any study and have rarely been applied to smaller species or those from high latitudes. Arctic foxes from the north and south of the peninsula, and those from rodent peak and trough density periods, are compared to assess impact of changes in food availability across space and time. Results indicate that microwear textures vary in dispersion, with more variation in texture complexity, including higher values (suggesting more consumption of bone), in the rodent-poor period in the north of Yamal. Gross wear scores and tooth breakage are also significantly higher for the north of Yamal than the south. These data together suggest that dental evidence can provide important insights into variation in the feeding ecology of Arctic foxes and potentially into the impacts of changes in food abundance across space and time.
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Data availability
All raw data presented in this study are available in the supplemental online materials. The original specimens are archived at the Arctic Research Station in Labytnangi, Russia.
References
Binder WJ, Van Valkenburgh B (2010) A comparison of tooth wear and breakage in Rancho La Brea sabertooth cats and dire wolves across time. J Vertebr Paleontol 30:255–261. https://doi.org/10.1080/02724630903413016
Bradley JA, Secord D, Prins L (1981) Age determination in the arctic fox (Alopex lagopus). Can J Zool 59:1976–1979. https://doi.org/10.1139/z81-269
Calandra I, Merceron G (2016) Dental microwear texture analysis in mammalian ecology. Mamm Rev 46:215–228. https://doi.org/10.1111/mam.12063
Christensen RHB (2019) ordinal—regression models for ordinal data. R package version 2019.12-10. https://CRAN.R-project.org/package=ordinal
Conover WJ, Iman RL (1981) Rank transformations as a bridge between parametric and nonparametric statistics. Am Stat 35:124–129. https://doi.org/10.1080/00031305.1981.10479327
Couve E, Osorio R, Schmachtenberg O (2013) The amazing odontoblast: activity, autophagy, and aging. J Dent Res 92:765–772. https://doi.org/10.1177/0022034513495874
DeSantis LRG (2016) Dental microwear textures: reconstructing diets of fossil mammals. Surf Topogr Metrol Prop 4:023002. https://doi.org/10.1088/2051-672X/4/2/023002
Ehrich D, Cerezo M, Rodnikova AY, Sokolova NA, Fuglei E, Shtro VG, Sokolov AA (2017) Vole abundance and reindeer carcasses determine breeding activity of Arctic foxes in low Arctic Yamal, Russia. BMC Ecol 17:32. https://doi.org/10.1186/s12898-017-0142-z
Eide NE, Stien A, Prestrud P, Yoccoz NG, Fuglei E (2012) Reproductive responses to spatial and temporal prey availability in a coastal Arctic fox population. J Anim Ecol 81:640–648. https://doi.org/10.1111/j.1365-2656.2011.01936.x
Flower LOH, Schreve DC (2014) An investigation of palaeodietary variability in European Pleistocene canids. Quat Sci Rev 96:188–203. https://doi.org/10.1016/j.quascirev.2014.04.015
Forbes BC et al (2016) Sea ice, rain-on-snow and tundra reindeer nomadism in Arctic Russia. Biol Lett. https://doi.org/10.1098/rsbl.2016.0466
Gharajehdaghipour T et al (2016) Arctic foxes as ecosystem engineers: increased soil nutrients lead to increased plant productivity on fox dens. Sci Rep 6:24020. https://doi.org/10.1038/srep24020
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. https://doi.org/10.1016/S0047-2484(86)80010-0
Henden JA, Yoccoz NG, Ims RA, Bardsen BJ, Angerbjorn A (2009) Phase-dependent effect of conservation efforts in cyclically fluctuating populations of arctic fox (Vulpes lagopus). Biol Conserv 142:2586–2592. https://doi.org/10.1016/j.biocon.2009.06.005
Hurvich CM, Tsai CL (1989) Regression and time series model selection in small samples. Biometrika 76:297–307. https://doi.org/10.1093/biomet/76.2.297
Ims RA, Killengreen ST, Ehrich D, Flagstad Ø, Hamel S, Henden JA, Jensvoll I, Yoccoz NG (2017) Ecosystem drivers of an Arctic fox population at the western fringe of the Eurasian Arctic. Polar Res. https://doi.org/10.1080/17518369.2017.1323621
IUCN (2009) Species and climate change. More than just polar bears. The IUCN Red List of Threatened Species. International Union for Conservation of Nature and Natural Resources, Gland, Switzerland
Krueger KL, Scott JR, Ungar PS (2008) Technical note: Dental microwear textures of “Phase I” and “Phase II” facets. Am J Phys Anthropol 137:485–490. https://doi.org/10.1002/ajpa.20928
Levene H (1960) Robust tests for equality of variances. In: Olkin I (ed) Contributions to probability and statistics. Stanford University Press, Palo Alto, pp 278–292
Mann SA, Van Valkenburgh B, Hayward MW (2017) Tooth fracture within the African carnivore guild: the influence of intraguild competition and resource availability. J Zool 303:261–269. https://doi.org/10.1111/jzo.12488
Pavlinin VN (1971) Mountain hare Lepus timidus L. Mammals of the Yamal and the Polar Urals. Proceedings of the Institute of Plant and Animal Ecology. Sverdlovsk 1:75–105
Pereleshin SD (1943) Winter fox food in the Yamal Okrug. Zool J 14:97–112
Prassack KA, DuBois J, Lázničková-Galetová M, Germonpré M, Ungar PS (2020) Dental microwear as a behavioral proxy for distinguishing between canids at the Upper Paleolithic (Gravettian) site of Předmostí, Czech Republic. J Archaeol Sci 115:105092. https://doi.org/10.1016/j.jas.2020.105092
R Core Team (2020) A language and environment for statistical computing. R Foundation for Statistical Computing
Riabitsev VK (2001) Birds of the Ural, Ural foothills and Western Siberia: a guide. Ural Univ. Press, Ekaterinburg, p 159
Schubert BW, Ungar PS, DeSantis LRG (2010) Carnassial microwear and dietary behaviour in large carnivorans. J Zool 280:257–263. https://doi.org/10.1111/j.1469-7998.2009.00656.x
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. https://doi.org/10.1016/j.jhevol.2006.04.006
Shtro VG (1995) The number of ptarmigan at wintering places in the mountains of the Polar Urals and the floodplain of the Lower Ob. In: Balakhonov VS (ed) Current state of flora and fauna of the Yamal Peninsula. pp 96–99
Shtro VG (2006) Notes on the behavior of the mountain hare in the tundras of Yamal. Sci Bull YANAO 1(38):173–174
Shtro VG (2009) The Arctic Fox of Yamal. Institute of Plant and Animal Ecology, Ural Branch of the Russian Academy of Sciences, Ekaterinburg, Russia
Smirnov VS (1960) Determination of age and age relations in mammals example of squirrel, muskrat and five types of predators. Problems of Flora and Fauna of the Urals. Proceedings of the Institute of Plant and Animal Ecology Sverdlovsk, UB RAS, 1960, 14:97–112
Sokolov AA, Sokolova NA, Ims RA, Brucker L, Ehrich D (2016) Emergent rainy winter warm spells may promote boreal expansion into the Arctic. Arctic 69:121–129. https://doi.org/10.14430/arctic4559
Sokolova NA et al (2014) Small rodents in the shrub tundra of Yamal (Russia): density dependence in habitat use? Mamm Biol 79:306–312. https://doi.org/10.1016/j.mambio.2014.04.004
Star H, Thevissen P, Jacobs R, Fieuws S, Solheim T, Willems G (2011) Human dental age estimation by calculation of pulp-tooth volume ratios yielded on clinically acquired cone beam computed tomography images of monoradicular teeth. J Forensic Sci 56:S77–S82. https://doi.org/10.1111/j.1556-4029.2010.01633.x
Tanis BP, DeSantis LRG, Terry RC (2018) Dental microwear textures across cheek teeth in canids: implications for dietary studies of extant and extinct canids. Palaeogeogr Palaeoclimatol Palaeoecol 508:129–138. https://doi.org/10.1016/j.palaeo.2018.07.028
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. https://doi.org/10.1002/ajpa.1330800405
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. https://doi.org/10.1002/ajpa.24000
Tumlison R, McDaniel VR (1984) Gray fox age classification by canine tooth pulp cavity radiographs. J Wildl Manag 48:228–231. https://doi.org/10.2307/3808477
Ungar PS (2009) Tooth form and function: insights into adaptation through the analysis of dental microwear. In: Koppe T, Meyer G, Alt KW (eds) Interdisciplinary dental morphology. Springer, Berlin, pp 38–43
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, Scott JR, Schubert BW, Stynder DD (2010) Carnivoran dental microwear textures: comparability of carnassial facets and functional differentiation of postcanine teeth. Mammalia 74:219–224. https://doi.org/10.1515/Mamm.2010.015
Van Valkenburgh B (1988) Carnivore dental adaptations and diet: a study of trophic diversity within guilds. In: Gittleman JL (ed) Carnivore behavior, ecology, and evolution. Cornell University Press, Ithaca, pp 410–436
Van Valkenburgh B (1989) Carnivore dental adaptations and diet: a study of trophic diversity within guilds. In: Gittleman JL (ed) Carnivore behavior, ecology and evolution, vol 1. Cornell University Press, Ithaca, pp 410–436
Van Valkenburgh B (2009) Costs of carnivory: tooth fracture in Pleistocene and recent carnivorans. Biol J Linn Soc 96:68–81. https://doi.org/10.1111/j.1095-8312.2008.01108.x
Van Valkenburgh B, Teaford MF, Walker A (1990) Molar microwear and diet in large carnivores: inferences concerning diet in the sabretooth cat, Smilodon fatalis. J Zool 222:319–340. https://doi.org/10.1111/j.1469-7998.1990.tb05680.x
Van Valkenburgh B, Peterson RO, Smith DW, Stahler DR, Vucetich JA (2019) Tooth fracture frequency in gray wolves reflects prey availability. Elife 8:e48628. https://doi.org/10.7554/eLife.48628
Acknowledgements
We are grateful to Dieter Piepenburg, Robert Losey, and two anonymous reviewers for comments and suggestions that helped us improve the final version of this paper. NAS, IF, AAS, AT, and AV were supported by the Russian Foundation for Basic Research (Grant Number 18-05-60261), the Russian Center of Development of the Arctic, “Yamal-LNG” company, and the Government of the Yamal Nenets Autonomous District. OG, NAS, and AAS were supported by the French Polar Institute (Program “1036 Interactions”) and PRC CNRS Russie (Program “ECCVAT”). The collaboration was developed with support from the US National Science Foundation (Award Number 1927793) to PSU. We thank Violetta Filippova and Kirill Shklyar for providing Fig. 1.
Funding
NAS, IF, AAS, AT, and AV were supported through a 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. OG, NAS, and AAS were supported by the French Polar Institute (Program “1036 Interactions”) and PRC CNRS Russie (Program “ECCVAT”). PSU developed the collaboration through support from US National Science Foundation Award No.: 1927793.
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PSU, AAS, and NAS conceived of the project. NAS, VS, IF, and AAS collected/processed specimens and generated metadata used in this paper. PSU, BVV, and ASP generated the dental data presented in this paper. PSU, DE, and BVV analyzed the data and PSU, BVV, AAS, NAS, DE, OG, BVV, ASP, AT, and AV wrote the paper.
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Ungar, P.S., Van Valkenburgh, B., Peterson, A.S. et al. Dental evidence for variation in diet over time and space in the Arctic fox, Vulpes lagopus. Polar Biol 44, 509–523 (2021). https://doi.org/10.1007/s00300-021-02821-8
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DOI: https://doi.org/10.1007/s00300-021-02821-8