Polar Biology

pp 1–7

Not only mosses: lemming winter diets as described by DNA metabarcoding

  • Eeva M. Soininen
  • Lucie Zinger
  • Ludovic Gielly
  • Nigel G. Yoccoz
  • John-Andre Henden
  • Rolf A. Ims
Short Note
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Abstract

The temporal dynamics of most tundra food webs are shaped by the cyclic population dynamics of lemmings. While processes during winter may be behind the recent disruptions of lemming cycles, lemming winter ecology is poorly known. We present here the first DNA metabarcoding data on the winter diet of Norwegian lemmings (Lemmus lemmus), based on feces collected after a winter of population increase. Prostrate willows, mosses, and graminoids dominated the species winter diet, indicating that the conventional idea of lemmings as moss-specialists should be revised. The behavior of lemming-plant models in theoretical studies is conditional on the assumptions of mosses being their main winter food item. As shrubs have been excluded from the framework of these models, incorporating them in future modeling studies should nuance our understanding on how plants affect lemmings. We also sampled diet of a few individuals found dead on top of the snow. These individuals had relatively empty stomachs and had, prior to death, relied heavily on mosses. This apparent lack of abundant good quality indicates spatial heterogeneity in local food availability during the population increase phase.

Keywords

Arctic Bryophyte Lemmus lemmus Prostrate Salix Snowbed Winter 

Supplementary material

300_2017_2114_MOESM1_ESM.pdf (186 kb)
Supplementary material 1 (PDF 185 KB)

References

  1. Bilodeau F, Gauthier G, Berteaux D (2013a) Effect of snow cover on the vulnerability of lemmings to mammalian predators in the Canadian Arctic. J Mammal 94(4):813–819CrossRefGoogle Scholar
  2. Bilodeau F, Kenney AJ, Gilbert BS, Hofer E, Gauthier G, Reid DG, Berteaux D, Krebs CJ (2013b) Evaluation of a technique to trap lemmings under the snow. Arctic 66(1):32–36CrossRefGoogle Scholar
  3. Boyer F, Mercier C, Bonin A, Le Bras Y, Taberlet P, Coissac E (2016) OBITOOLS: a UNIX-inspired software package for DNA metabarcoding. Mol Ecol Resour 16(1):176–182CrossRefPubMedGoogle Scholar
  4. 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 5:4132–4140CrossRefPubMedPubMedCentralGoogle Scholar
  5. Duchesne D, Gauthier G, Berteaux D (2011) Habitat selection, reproduction and predation of wintering lemmings in the Arctic. Oecologia 167(4):967–980CrossRefPubMedGoogle Scholar
  6. Gilg O, Sittler B, Hanski I (2009) Climate change and cyclic predator-prey population dynamics in the high Arctic. Glob Chang Biol 15 (11):2634–2652CrossRefGoogle Scholar
  7. Hansson L (1969) Spring populations of small mammals in central Swedish Lapland in 1964–68. Oikos 20:431–450CrossRefGoogle Scholar
  8. Ims RA, Fuglei E (2005) Trophic interaction cycles in tundra ecosystems and the impact of climate change. Bioscience 55:311–322CrossRefGoogle Scholar
  9. Ims RA, Yoccoz NG, Killengreen ST (2011) Determinants of lemming outbreaks. P Natl Acad Sci USA 108:1970–1974CrossRefGoogle Scholar
  10. Ims RA, Jepsen JU, Stien A, Yoccoz NG (2013) Science plan for COAT: climate ecological observatory for Arctic Tundra. Fram Centre Report Series, vol. 1. Fram Centre, TromsøGoogle Scholar
  11. Kalela O, Koponen T, Lind EA, Skarén U, Tast J (1961) Seasonal change of habitat in the Norwegian lemming Lemmus lemmus (L.). Ann Acad Sci Fenn A4 55:1–72Google Scholar
  12. 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 456:93–97CrossRefPubMedGoogle Scholar
  13. Koshkina TV (1961) New data on the nutrition of the Norwegian lemming (Lemmus lemmus) (in Russian). Byulletin Moskouskogo Obschchestua Ispyt Prir Otdel Biol 66:15–31Google Scholar
  14. Kowalczyk R, Taberlet P, Coissac E, Valentini A, Miquel C, Kaminski T, Wójcik JM (2011) Influence of management practices on large herbivore diet—case of European bison in Bialowiez a primeval forest (Poland). For Ecol Manag 261:821–828CrossRefGoogle Scholar
  15. Moen J, Lundberg PA, Oksanen L (1993) Lemming grazing on snowbed vegetation during a population peak, Northern Norway. Arct Alp Res 25:130–135CrossRefGoogle Scholar
  16. Nakahara F, Ando H, Ito H, Murakami A, Morimoto N, Yamasaki M, Takayanagi A, Isagi Y (2015) The applicability of DNA barcoding for dietary analysis of sika deer. DNA Barcodes 3:200–206CrossRefGoogle Scholar
  17. Newmaster SG, Thompson ID, Steeves RAD, Rodgers AR, Fazekas AJ, Maloles JR, McMullin RT, Fryxell JM (2013) Examination of two new technologies to assess the diet of woodland caribou: video recorders attached to collars and DNA barcoding. Can J For Res 43(10):897–900. doi:10.1139/cjfr-2013-0108 CrossRefGoogle Scholar
  18. Oksanen T, Oksanen L, Dahlgren J, Olofsson J (2008) Arctic lemmings, Lemmus spp. and Dicrostonyx spp.: integrating ecological and evolutionary perspectives. Evol Ecol Res 10:415–434Google Scholar
  19. Olofsson J, Tommervik H, Callaghan TV (2012) Vole and lemming activity observed from space. Nat Clim Chang 2(12):880–883CrossRefGoogle Scholar
  20. Pompanon F, Deagle BE, Symondson WOC, Brown DS, Jarman SN, Taberlet P (2012) Who is eating what: diet assessment using next generation sequencing. Mol Ecol 21:1931–1950CrossRefPubMedGoogle Scholar
  21. Saetnan ER, Gjershaug JO, Batzli GO (2009) Habitat use and diet composition of Norwegian lemmings and field voles in Central Norway. J Mammal 90(1):183–188CrossRefGoogle Scholar
  22. Soininen EM (2012) Interactions between small rodents and their food plants in tundra habitats (PhD thesis). University of Tromsø, Tromsø, NorwayGoogle Scholar
  23. Soininen EM, Valentini A, Coissac E, Miquel C, Gielly L, Brochmann C, Brysting AK, Sonstebo JH, Ims RA, Yoccoz NG, Taberlet P (2009) Analysing diet of small herbivores: the efficiency of DNA barcoding coupled with high-throughput pyrosequencing for deciphering the composition of complex plant mixtures. Front Zool 6:16. doi:10.1186/1742-9994-6-16 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Soininen EM, Zinger L, Gielly L, Bellemain E, Bråthen KA, Brochmann C, Epp LS, Gussarova G, Hassel K, Henden J-A, Killengreen ST, Rämä T, Stenøien HK, Yoccoz NG, Ims RA (2013) Shedding new light on the diet of Norwegian lemmings: DNA metabarcoding of stomach content. Polar Biol 36:1069–1076CrossRefGoogle Scholar
  25. 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 Healt S 50 (3):361–381CrossRefGoogle Scholar
  26. Soininen EM, Gauthier G, Bilodeau F, Berteaux D, Gielly L, Taberlet P, Gussarova G, Bellemain E, Hassel K, Stenøien HK, Epp L, Schrøder-Nielsen A, Brochmann C, Yoccoz NG (2015a) Highly overlapping winter diet in two sympatric lemming species revealed by DNA metabarcoding. PLoS ONE 10(1):e0115335. doi:10.1371/journal.pone.0115335 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Soininen EM, Gauthier G, Bilodeau F, Berteaux D, Gielly L, Taberlet P, Gussarova G, Bellemain E, Hassel K, Stenøien HK, Epp L, Schrøder-Nilsen A, Brochmann C, Yoccoz NG (2015b) Data from: highly overlapping winter diet in two sympatric lemming species revealed by DNA metabarcoding. Dryad Data Repos. doi:10.5061/dryad.4rr39 Google Scholar
  28. Sønstebø JH, Gielly L, Brysting A, Elven R, Edwards M, Haile J, Willerslev E, Coissac E, Roiux D, Sannier J, Taberlet P, Brochmann C (2010) Using next-generation sequencing for molecular reconstruction of past Arctic vegetation and climate. Mol Ecol Resour 10:1009–1018CrossRefPubMedGoogle Scholar
  29. Stoddart DM (1967) A note on the food of the Norway lemming. J Zool 151:211–213CrossRefGoogle Scholar
  30. Taberlet P, Coissac E, Pompanon F, Gielly L, Miquel C, Valentini A, Vermat T, Corthier G, Brochmann C, Willerslev E (2007) Power and limitations of the chloroplast trnL (UAA) intron for plant DNA barcoding. Nucleic Acids Res 35(3):e14CrossRefPubMedGoogle Scholar
  31. Taberlet P, Coissac E, Hajibabaei M, Rieseberg LH (2012) Environmental DNA. Mol Ecol 21:1789–1793CrossRefPubMedGoogle Scholar
  32. Tast J (1991) Will the Norwegian lemming become endangered if climate becomes warmer? Arct Alp Res 23:53–60CrossRefGoogle Scholar
  33. Turchin P, Batzli G (2001) Availability of food and the population dynamics of arvicoline rodents. Ecology 82(6):1521–1534CrossRefGoogle Scholar
  34. Turchin P, Oksanen L, Ekerholm P, Oksanen T, Henttonen H (2000) Are lemmings prey or predators? Nature 405:562–565CrossRefPubMedGoogle Scholar
  35. Virtanen R (2000) Effects of grazing on above-ground biomass on a mountain snowbed, NW Finland. Oikos 90(2):295–300CrossRefGoogle Scholar
  36. Willerslev E, Davison J, Moora M, Zobel M, Coissac E, Edwards ME, Lorenzen ED, Vestergard M, Gussarova G, Haile J et al (2014a) Fifty thousand years of Arctic vegetation and megafaunal diet. Nature 506(7486):47–51CrossRefPubMedGoogle Scholar
  37. Willerslev E, Davison J, Moora M, Zobel M, Coissac E, Edwards ME, Lorenzen ED, Vestergård M, Gussarova G, Haile J, et al. (2014b) Data from: Fifty thousand years of arctic vegetation and megafaunal diet. Dryad Data Repos. doi:10.5061/dryad.ph8s5 Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Department of Arctic and Marine BiologyUiT – The Arctic University of NorwayTromsøNorway
  2. 2.Laboratoire d’Ecologie AlpineUMR CNRS-UGA-USMB 5553, Université Grenoble AlpesGrenoble Cedex 9France
  3. 3.Université Toulouse 3 Paul Sabatier, CNRS, ENFA, UMR 5174 EDBToulouseFrance

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