Skip to main content
Log in

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

  • Short Note
  • Published:
Polar Biology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

References

  • 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):813–819

    Article  Google Scholar 

  • 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):32–36

    Article  Google Scholar 

  • 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):176–182

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Duchesne D, Gauthier G, Berteaux D (2011) Habitat selection, reproduction and predation of wintering lemmings in the Arctic. Oecologia 167(4):967–980

    Article  PubMed  Google Scholar 

  • Gilg O, Sittler B, Hanski I (2009) Climate change and cyclic predator-prey population dynamics in the high Arctic. Glob Chang Biol 15 (11):2634–2652

    Article  Google Scholar 

  • Hansson L (1969) Spring populations of small mammals in central Swedish Lapland in 1964–68. Oikos 20:431–450

    Article  Google Scholar 

  • Ims RA, Fuglei E (2005) Trophic interaction cycles in tundra ecosystems and the impact of climate change. Bioscience 55:311–322

    Article  Google Scholar 

  • Ims RA, Yoccoz NG, Killengreen ST (2011) Determinants of lemming outbreaks. P Natl Acad Sci USA 108:1970–1974

    Article  CAS  Google Scholar 

  • 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, Tromsø

    Google Scholar 

  • 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 55:1–72

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Koshkina TV (1961) New data on the nutrition of the Norwegian lemming (Lemmus lemmus) (in Russian). Byulletin Moskouskogo Obschchestua Ispyt Prir Otdel Biol 66:15–31

    Google Scholar 

  • 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 261:821–828

    Article  Google Scholar 

  • Moen J, Lundberg PA, Oksanen L (1993) Lemming grazing on snowbed vegetation during a population peak, Northern Norway. Arct Alp Res 25:130–135

    Article  Google Scholar 

  • 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 3:200–206

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Oksanen T, Oksanen L, Dahlgren J, Olofsson J (2008) Arctic lemmings, Lemmus spp. and Dicrostonyx spp.: integrating ecological and evolutionary perspectives. Evol Ecol Res 10:415–434

    Google Scholar 

  • Olofsson J, Tommervik H, Callaghan TV (2012) Vole and lemming activity observed from space. Nat Clim Chang 2(12):880–883

    Article  Google Scholar 

  • 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 21:1931–1950

    Article  CAS  PubMed  Google Scholar 

  • 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):183–188

    Article  Google Scholar 

  • Soininen EM (2012) Interactions between small rodents and their food plants in tundra habitats (PhD thesis). University of Tromsø, Tromsø, Norway

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 36:1069–1076

    Article  Google Scholar 

  • 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):361–381

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 

  • 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 10:1009–1018

    Article  PubMed  Google Scholar 

  • Stoddart DM (1967) A note on the food of the Norway lemming. J Zool 151:211–213

    Article  Google Scholar 

  • 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):e14

    Article  PubMed  Google Scholar 

  • Taberlet P, Coissac E, Hajibabaei M, Rieseberg LH (2012) Environmental DNA. Mol Ecol 21:1789–1793

    Article  CAS  PubMed  Google Scholar 

  • Tast J (1991) Will the Norwegian lemming become endangered if climate becomes warmer? Arct Alp Res 23:53–60

    Article  Google Scholar 

  • Turchin P, Batzli G (2001) Availability of food and the population dynamics of arvicoline rodents. Ecology 82(6):1521–1534

    Article  Google Scholar 

  • Turchin P, Oksanen L, Ekerholm P, Oksanen T, Henttonen H (2000) Are lemmings prey or predators? Nature 405:562–565

    Article  CAS  PubMed  Google Scholar 

  • Virtanen R (2000) Effects of grazing on above-ground biomass on a mountain snowbed, NW Finland. Oikos 90(2):295–300

    Article  Google Scholar 

  • 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):47–51

    Article  CAS  PubMed  Google Scholar 

  • 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 

Download references

Acknowledgements

We thank Siw Killengreen, Geir Vie, Sandra Hamel, Kristoffer H. Juell, Francisco Javier Ancin Murguzur, and Ingrid Jensvoll for collecting samples in the field; Christian Miquel, Delphine Rioux and Alice Valentini help with the laboratory; Eric Coissac for help with the bioinformatics analyses; and Eivind Flittie Kleiven for help with checking snow melt dates. The work of Eeva M. Soininen was supported by Oskar Huttunen foundation and the Fram Centre through the Climate-Ecological Observatory for Arctic Tundra (COAT). Sample collection was funded by the Research Council of Norway (project EcoFinn).

Funding

Funding was provided by Oskar Huttunen Foundation (Grant for doctoral studies) and Norwegian Research Council (Grant No. 184140).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Eeva M. Soininen.

Ethics declarations

Conflict of interest

We would like to mention that Ludovic Gielly is one of the co-inventors of a patent concerning g-h primers and the subsequent use of the P6 loop of the chloroplast trnL (UAA) intron for plant identification using degraded template DNA. These patents only restrict commercial applications and have no impact on the use of this locus by academic researchers.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 185 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Soininen, E.M., Zinger, L., Gielly, L. et al. Not only mosses: lemming winter diets as described by DNA metabarcoding. Polar Biol 40, 2097–2103 (2017). https://doi.org/10.1007/s00300-017-2114-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00300-017-2114-3

Keywords

Navigation