Foraging plasticity allows a large herbivore to persist in a sheltering forest habitat: DNA metabarcoding diet analysis of the European bison
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.
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Present address: SPYGEN, Savoie Technolac - BP 274, Le Bourget-du-Lac 73375, France.