Shedding new light on the diet of Norwegian lemmings: DNA metabarcoding of stomach content
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Lemmings are key herbivores in many arctic food webs, and their population dynamics have major impacts on the functioning of tundra systems. However, current knowledge of lemming diet is limited, hampering evaluation of lemming–vegetation interactions. This lack of knowledge is mainly due to methodological challenges, as previously used microhistological methods result in large proportions of poorly resolved plant taxa. We analyzed diets of Norwegian lemmings (Lemmus lemmus) in three different habitats using a new method, DNA metabarcoding of stomach contents. To achieve detailed information on ingested vascular plants, bryophytes, and fungi, we amplified short fragments of chloroplast DNA (for plants; P6 loop of the trnL intron) and nuclear ribosomal DNA (for fungi; ITS1-region). Our results revealed that lemming diets were dominated by grasses, mainly Avenella flexuosa, and mosses, mainly Dicranum spp., but that a variety of other food items were also eaten. Vascular plant composition of the diets differed between heath, meadow, and wetland habitats, whereas bryophyte composition did not. Also, a variety of fungal taxa were retrieved, but as most of the identified taxa belong to micromycetes, they were unlikely to be consumed as food. The role of fungi in the diet of lemmings remains to be investigated. We suggest that there may be substantial variation between habitats and regions in lemming diet.
KeywordsSmall rodents Lemmus lemmus Tundra Herbivore trnL approach Fungi
We thank Arne-Petter Sarre, Alfred Ørjebo, and all field assistants for collecting lemming samples in 2007; Torbjørn Alm, Knut Rydgren, and Leif Einar Støveren for taxonomic expertise; Christian Miquel, Delphine Rioux, Alice Valentini, Virginia Mirré, and Audun Schrøder-Nielsen for technical assistance in the laboratory; Eric Coissac and Frédéric Boyer for help in data handling; Pierre Taberlet for fruitful discussions and two anonymous reviewers for valuable comments that have improved the manuscript. This project was funded by the Research Council of Norway (Ecosystem Finnmark) and Oskar Huttunen Fond (PhD scholarship for EMS). Funding for building the taxonomic reference libraries was obtained from the Research Council of Norway (the BarFrost project, Grant No. 191627/V40 to CB).
Conflict of interest
We would like to mention that L.G. 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.
- Batzli GO (1993) Food selection by lemmings. In: Stensetch NC, Ims RA (eds) The biology of lemmings, 1st edn. Academic Press, London, pp 281–301Google Scholar
- Epp L, Boessenkool S, Bellemain E, Haile J, Esposito A, Riaz T, Erseus C, Gusarov VI, Edwards ME, Johnsen A, Steinøien HK, Hassel K, Kauserud H, Yoccoz NG, Bråthen KA, Willerslev E, Taberlet P, Coissac E, Brochmann C (2012) New environmental metabarcodes for analysing soil DNA: potential for studying past and present ecosystems. Mol Ecol 21:1821–1833PubMedCrossRefGoogle Scholar
- Eskelinen O (2002) Diet of the wood lemming Myopus schisticolor. Ann Zool Fenn 39:49–57Google Scholar
- Hansen L, Knudsen H (eds) (1992) Nordic macromycetes vol. 2. Polyporales, Boletales, Agaricales, Russulales. Nordsvamp, CopenhagenGoogle Scholar
- Hassel K, Prestø T, Schmidt NM (2012) Bryophyte diversity in high and low arctic Greenland. Establishment of permanent monitoring transects and bryophyte and bryophyte mapping in Zackenberg and Kobbefjord 2009–2010. Scientific Report from DCE—Danish Centre for Environment and Energy No. 2/. Aarhus University, Roskilde, DenmarkGoogle Scholar
- Hill MO, Bell N, Bruggeman-Nannenga MA, Brugues M, Cano MJ, Enroth J, Flatberg KI, Frahm JP, Gallego MT, Garilleti R, Guerra J, Hedenas L, Holyoak DT, Hyvonen J, Ignatov MS, Lara F, Mazimpaka V, Munoz J, Söderström L (2006) An annotated checklist of the mosses of Europe and Macaronesia. J Bryol 28:198–267CrossRefGoogle 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 A IV 55:1–72Google Scholar
- Koshkina TV (1961) New data on the nutrition of the Norwegian lemming (Lemmus lemmus). Bull Mosk Obshch Ispytal Prirod 66:15–31 (in Russian)Google Scholar
- Krebs CJ, Danell K, Angerbjörn A, Agrell J, Berteaux D, Bråthen KA, Danell O, Erlinge S, Fedorov V, Fredga K, Hjältén J, Högstedt G, Jónsdóttir IS, Kenney AJ, Kjellén N, Nordin T, Roininen H, Svensson M, Tannerfeldt M, Wiklund C (2003) Terrestrial trophic dynamics in the Canadian Arctic. Can J Zool 81:827–843CrossRefGoogle Scholar
- Morris DW, Davidson DL, Krebs CJ (2000) Measuring the ghost of competition: insights from density-dependent habitat selection on the co-existence and dynamics of lemmings. Evol Ecol Res 2:41–67Google 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 10:415–434Google Scholar
- Ravolainen VT, Bråthen KA, Ims RA, Yoccoz NG, Soininen EM (2013) Shrub patch configuration at the landscape scale is related to diversity of adjacent herbaceous vegetation. Plant Ecol Div. doi: 10.1080/17550874.2013.773104
- Soininen EM, Valentini A, Coissac E, Miquel C, Gielly L, Brochmann C, Brysting AK, Sonstebo JH, Ims RI, 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 PubMedCrossRefGoogle Scholar
- Stoddart DM (1967) A note on the food of the Norway lemming. J Zool 151:211–213Google Scholar
- White T, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innins MA, Gelfand DH, Sninski JJ, White TJ (eds) PCR-protocols a guide to methods and applications. Academic Press, San Diego, pp 315–322Google Scholar