Foraging plasticity allows a large herbivore to persist in a sheltering forest habitat: DNA metabarcoding diet analysis of the European bison

https://doi.org/10.1016/j.foreco.2019.117474Get rights and content

Highlights

  • European bison fed on 105 plant taxa during growing season in Białowieża Forest.

  • Woody species (59.4% of DNA sequences) and forbs (33.6%) dominated in bison diet.

  • The diversity of plants eaten by bison increased with increasing food availability.

  • Bison continuously adjusts its diet with seasonal availability of non-grass vegetation.

  • Diet plasticity and use of forest openings allow bison to persist in sheltering forest habitats.

Abstract

Large herbivores that survived the Pleistocene/Holocene transition are hypothesized to have been forced to take refuge, as a result of environmental changes and human pressure, into forest habitats. Today, there is an open question of the degree to which extant large herbivores are well adapted to the forests that allowed for the herbivores’ persistence. We studied the diet of European bison (Bison bonasus), the largest terrestrial mammal in Europe, to gain insight into the foraging behaviour of a large herbivore, that appears to be primarily adapted to grazing but has been restored to forested habitats. The study population resided in the Białowieża Primeval Forests, Poland. DNA-based analysis of faecal samples revealed strong seasonal and spatial patterns in bison foraging, consistent between sexes. Bison fed on at least 105 different plant taxa. Woody species constituted 59.4% of DNA sequences, and forbs 33.6%. The two most abundant taxa were raspberry (Rubus idaeus) and European hornbeam (Carpinus betulus), which together comprised 31.0% of the dietary sequences and occurred in over 80% of faecal samples. Seasonally, the diversity of plants eaten by bison increased with increasing food availability. During high plant biomass in summer, bison consumed up to 40 different plant taxa. There was little overlap in the composition of the diet from month to month, reflecting the strong seasonality of vegetation abundance and/or its dietary quality. The results indicate high plasticity in bison foraging strategies and response to seasonal changes in biomass and the species composition of plants. Bison are browsers which continuously adjusts their diet with seasonal availability of easily digestible non-grass vegetation. We propose that dietary plasticity and micro-selection for open habitats (gaps and river valleys) within a forested landscape allowed bison to persist in sheltering forest habitats during the Holocene and accommodate to forest environments during species restoration.

Introduction

Most large Northern Hemisphere Pleistocene herbivores went extinct before the Holocene (Wroe et al., 2004, Cooper et al., 2015). European species that survived such as the European bison (Bison bonasus), aurochs (Bos primigenius) and moose (Alces alces), gradually disappeared from European landscapes in response to environmental changes and human impact (Benecke, 2005, Schmölcke and Zachos, 2005, Marchant et al., 2009, Turvey, 2009, Mona et al., 2010). Climate and environmental changes, over-exploitation, habitat transformation and fragmentation consistently affect wildlife (Chevin et al., 2010). Those changes were especially evident during the Holocene, when many species of animals, especially herbivores, faced dramatic environmental change (Huntley, 1990, Crees and Turvey, 2014, Hoogakker et al., 2016). Isotopic reconstruction of the habitat use by large herbivores, including European bison, shows a shift from more open habitats in the early and pre-Neolithic Holocene to forested habitats during the Neolith and late Holocene (Hofman-Kamińska et al., 2019). Adaptation to changing conditions and ecological plasticity were probably the features that favored survival (Hofman-Kamińska et al., 2019). Some species, such as European bison – the largest terrestrial mammal that remained in Europe, survived in forest habitats (Krasińska and Krasiński, 2013). However, its evolutionary ancestry, morphological adaptations (wide muzzle, hypsodont teeth) and habitat selection indicate that the species evolved as an open or mixed habitat dweller (Mendoza and Palmqvist, 2008, Kerley et al., 2012, Bocherens et al., 2015) and can be recognised as a refugee species (Kerley et al., 2012). To survive in forests, such species would not only need to adapt to a new suite of plant species, but also strong seasonal changes in biomass and plant species availability characteristic of temperate forests (Bradshaw et al., 2003, Hofman-Kamińska et al., 2018a, Hofman-Kamińska et al., 2018b).

The majority of mammalian herbivores are generalists (Freeland, 1991), consuming a large range of different plants of varying quality. Understanding dietary specialization in herbivores has theoretical and practical implications in ecology (Shipley et al., 2009, Valdes-Correcher et al., 2018). As stated by optimal foraging theory, animals will optimize their foraging efficiency through trade-off between food profitability and searching time: optimal diet will include fewer items if the availability of profitable food increases, because the search time for such food is shorter (MacArthur and Pianka, 1966, Pulliam, 1974, Krebs and Davies, 1978). Based on this theory we can predict that animals should prefer more profitable foods and be more selective when high-ranking food is common.

Previous studies showed that European bison can be considered a mixed feeder or browser, with a significant component of herbaceous plants in its diet (67–97%) (Borowski and Kossak, 1972, Gębczyńska et al., 1991). Winter diet of bison is strongly shaped by access to supplementary feeding (mainly hay) (Kowalczyk et al., 2011). Isotopic evidence showed that pattern of habitat use and diet of bison populations are strongly influenced by the habitat structure (proportion of forest cover) (Hofman-Kamińska et al., 2018a, Hofman-Kamińska et al., 2018b). It indicates some plasticity of bison in accommodation to forest habitats, however supplementary feeding used in many places or seasonal migrations to agriculture areas allow bison to cope with seasonality and late autumn-early spring shortage of forage in forests (Hofman-Kamińska et al., 2018a, Hofman-Kamińska et al., 2018b, Hofman-Kamińska and Kowalczyk, 2012, Kowalczyk et al., 2011, Kowalczyk et al., 2013).

European bison are characterized by large sexual dimorphism (Krasińska and Krasiński, 2002). Males are on average 50% larger than females, which may indicate niche differentiation predicted by the Jarman-Bell principle (Geist, 1974). It states that larger animals can or must tolerate lower quality diets (high content of fiber), because of their lower metabolism requirement/gut capacity ratio (Demment and van Soest, 1985). The concept has mainly so far been explored in ruminants on an inter-specific level (Müller et al., 2013). However, it was found that the Jarman-Bell principle also operates at the intraspecific level and may be an important factor influencing sexual segregation (Pérez-Barbería et al., 2002).

In this paper we investigated the diet of European bison in one of the last pristine temperate forest in Europe (Latałowa et al., 2015), during the growing season and not influenced by supplementary feeding. This allowed examination of the selection of vegetation by European bison in order to determine the degree to which extant large herbivores utilise forest habitats which might be key for long-term persistence. We analysed sexual, seasonal and spatial variation of bison diet and the influence of food availability on the diet diversity. We hypothesised that European bison are characterised by a wide food niche at low food availability and become more selective during high food abundance as predicted by optimal foraging theory (MacArthur and Pianka, 1966). We also asked if large sexual dimorphism in bison influence the diet of males and females as stated by the Jarman-Bell principle (Geist, 1974). We used a DNA-based method of diet analysis (Kowalczyk et al., 2011, Hibert et al., 2013, Bergmann et al., 2015), to analyse large amounts of faecal samples collected in different months.

Section snippets

Study area

We investigated bison diet in the Białowieża Primeval Forest (BPF) - one of the best-preserved temperate lowland forests in Europe, located on both sides of the border between Poland and Belarus (52°35′-52°55′N, 23°30′-24°00′E). The study area included both strictly protected Białowieża National Park (100 km2) and the exploited forests with numerous reserves (520 km2). The continuity of the BPF is interrupted by natural gaps in protected areas and small clear cutting areas in the exploited

Raw dataset description

The NGS raw read data contained circa 5.7 million reads exhibiting the correct tags and primers. After the seven steps of data pre-processing, 3,640,452 reads were conserved. Eleven samples exhibited no sequences, for the 181 remaining, the read counts were relatively evenly distributed (mean = 20112, 95% of the samples get between 2340 and 47,483 reads). At the sample level, to exclude possible spurious PCR we exclude: i) eighteen samples exhibiting less than 7000 reads, ii) two atypical

Discussion

We used the metabarcoding approach to study the dietary composition of European bison. One concern with metabarcoding dietary reconstruction is that it might not serve as an accurate proxy for plant species intake (e.g. Deagle et al., 2014, Nichols et al., 2016, Piñol et al., 2018). Here, trnL is a chloroplast marker, which would provide a different signal than a mitochondrial or nuclear marker. It has been reasoned that the relative abundance of sequences from trnL, being a chloroplast

Acknowledgements

We thank Dr. Agata Kawałko for laboratory work and her help in preparing the trnL sequences of plant species from the Białowieża Primeval Forest for a trnL reference library. Ms Eleanor Stockwell and Mr Kingsley Hunt kindly improved English in the manuscript.

Fundings

The study was funded by grant no NN304 253435 of the Ministry of Science and Higher Education, Poland.

References (87)

  • T.C. Schneider et al.

    Resting site selection by large herbivores - The case of European bison (Bison bonasus) in Białowieża Primeval Forest

    Mamm. Biol.

    (2013)
  • B.M. Adhikari et al.

    Comparison of nutritional properties of Stinging nettle (Urtica dioica) flour with wheat and barley flours

    Food Sci. Nutr.

    (2016)
  • M.J. Anderson

    A new method for non-parametric multivariate analysis of variance

    Austral. Ecol.

    (2001)
  • M. Barančeková

    The roe deer diet: Is floodplain forest optimal habitat?

    Folia Zool.

    (2004)
  • N. Benecke

    Animal husbandry and hunting in pre- and early history on Buyukkaya in Bogazkoy-Hattusa, Central Anatolia

    Environ. Archaeol.

    (2005)
  • C.M. Bergman et al.

    Ungulate foraging strategies: energy maximizing or time minimizing?

    J. Anim. Ecol.

    (2001)
  • G.T. Bergmann et al.

    Seasonal shifts in diet and gut microbiota of the American bison (Bison bison)

    PLoS ONE

    (2015)
  • E. Bernadzki et al.

    Compositional dynamics of natural forests in the Białowieża National Park, northeastern Poland

    J. Veg. Sci.

    (1998)
  • W. Biel et al.

    The nutritional value of leaves of selected berry species

    Scientia Agricola

    (2017)
  • A. Bobiec

    The mosaic diversity of field layer vegetation in the natural and exploited forests of Białowieża

    Plant Ecol.

    (1998)
  • H. Bocherens et al.

    European bison as a refugee species? Evidence from isotopic data on early Holocene bison and other large herbivores in Northern Europe

    PLoS ONE

    (2015)
  • S. Borowski et al.

    The natural food preferences of the European bison in seasons free of snow cover

    Acta Theriol.

    (1972)
  • F. Boyer et al.

    OBITOOLS: a UNIX-inspired software package for DNA metabarcoding

    Mol. Ecol. Resour.

    (2016)
  • D.I. Bransby et al.

    Disk meter for rapid estimation of herbage yield in grazing trials

    Agron. J.

    (1977)
  • L.M. Chevin et al.

    Adaptation, plasticity, and extinction in a changing environment: Towards a predictive theory

    PLoS Biol.

    (2010)
  • A. Cooper et al.

    Abrupt warming events drove Late Pleistocene Holarctic megafaunal turnover

    Science

    (2015)
  • J.M. Craine et al.

    Climatic warming and the future of bison as grazers

    Sci. Rep.

    (2015)
  • K. Daleszczyk et al.

    Habitat structure, climatic factors, and habitat use by European bison (Bison bonasus) in Polish and Belarusian parts of the Bialowieza Forest, Poland

    Can. J. Zool.

    (2007)
  • B.E. Deagle et al.

    DNA metabarcoding and the cytochrome c oxidase subunit I marker: not a perfect match

    Biol. Lett.

    (2014)
  • M.L. Delignette-Muller et al.

    fitdistrplus: An R package for fitting distributions

    J. Stat. Softw.

    (2015)
  • M.W. Demment et al.

    A nutritional explanation for body-size patterns of ruminant and nonruminant herbivores

    Am. Nat.

    (1985)
  • S. Dray et al.

    The ade4 package: Implementing the duality diagram for ecologists

    J. Stat. Softw.

    (2007)
  • S. Dumolin et al.

    Inheritance of chloroplast and mitochondrial genomes in pedunculate oak investigated with an efficient PCR method

    Theor. Appl. Genet.

    (1995)
  • J.B. Faliński

    Vegetation Dynamics in Temperate Lowland Primeval Forests. Ecological Studies in Białowieża Forest

    (1986)
  • G.F. Ficetola et al.

    An in silico approach for the evaluation of DNA barcodes

    BMC Genomics

    (2010)
  • D. Fortin et al.

    The temporal scale of foraging decisions in bison

    Ecology

    (2002)
  • W.J. Freeland

    Plant secondary metabolites. Biochemical evolution with herbivore

  • S.D. Gad et al.

    Diet composition and quality in Indian bison (Bos gaurus) based on fecal analysis

    Zool. Sci.

    (2011)
  • M. Gautier et al.

    Deciphering the wisent demographic and adaptive histories from individual whole-genome sequences

    Mol. Biol. Evol.

    (2016)
  • C. Gebert et al.

    Variations of diet composition of Red Deer (Cervus elaphus L.) in Europe

    Mammal Rev.

    (2001)
  • V. Geist

    On the relationship of social evolution and ecology in ungulates

    Am. Zool.

    (1974)
  • Z. Gębczyńska et al.

    Food eaten by the free-living European bison in Białowieża Forest

    Acta Theriol.

    (1991)
  • F. Hibert et al.

    Unveiling the diet of elusive rainforest herbivores in next generation sequencing era? The tapir as a case study

    PLoS ONE

    (2013)
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    Present address: SPYGEN, Savoie Technolac - BP 274, Le Bourget-du-Lac 73375, France.

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