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. Author manuscript; available in PMC: 2019 May 17.
Published in final edited form as: Glob Chang Biol. 2019 Feb 28;25(5):1808–1819. doi: 10.1111/gcb.14587

Different effects of alpine woody plant expansion on domestic and wild ungulates

Johan Espunyes 1, Miguel Lurgi 2, Ulf Büntgen 3,4,5,6, Jordi Bartolomé 7, Juan Antonio Calleja 8,9, Arturo Gálvez-Cerón 1,10, Josep Peñuelas 9,11, Bernat Claramunt-López 12,13, Emmanuel Serrano 1
PMCID: PMC6522367  EMSID: EMS82082  PMID: 30737872

Abstract

Changes in land-use and climate affect the distribution and diversity of plant and animal species at different spatiotemporal scales. The extent to which species-specific phenotypic plasticity and biotic interactions mediate organismal adaptation to changing environments, however, remains poorly understood. Woody plant expansion is threatening the extent of alpine grasslands worldwide, and evaluating and predicting its effects on herbivores is of crucial importance. Here, we explore the impact of shrubification on the feeding efficiency of Pyrenean chamois (Rupicapra p. pyrenaica), as well as on the three most abundant coexisting domestic ungulate species: cattle, sheep and horses. We use observational diet composition from May to October and model different scenarios of vegetation availability where shrubland and woodland proliferate at the expense of grassland. We then predicted if the four ungulate species could efficiently utilize their food landscapes with their current dietary specificities measuring their niche breath in each scenario. We observed that the wild counterpart, due to a higher trophic plasticity, is less disturbed by shrubification compared to livestock, which rely primarily on herbaceous plants and will be affected 3.6 times more. Our results suggest that mixed feeders, such as chamois, could benefit from fallow landscapes, and that mountain farmers are at a growing economic risk worldwide due to changing land-use practices and climate conditions.

Keywords: diet preference, free-ranging livestock, habitat change, herbivory, mountain ecosystems, Pyrenean chamois, shrubification

1. Introduction

Environmental and climatic changes are affecting biological and ecological systems across the globe at alarming rates (Steffen, Sanderson, & Tyson, 2005). These trends influence fauna and flora in many ways, from habitat degradation to distributional range shifts, as well as phenological mismatch (Parmesan & Yohe, 2003; Pereira et al., 2010; Root et al., 2003). In fact, global land-use and climatic changes, through their influence on different aspects of the biology and ecology of species, have caused numerous extinctions (Vitousek, Mooney, Lubchenco, & Melillo, 1997), with models predicting an intensification of these trends over the next century (Loarie et al., 2009). Specialist species are predicted to decline at a faster rate due to their limited adaptive potential within their narrow environmental tolerances (Thuiller, Lavorel, & Araújo, 2005; Morrison, Estrada, & Early, 2018). Understanding the species-specific potential and limitation to cope with global change is thus a central aspect of timely conservation studies (Charmantier et al., 2008; Nussey, Clutton-Brock, Albon, Pemberton, & Kruuk, 2005).

In this context, evaluating and predicting the impact of global change on wild herbivores has become a conservation priority globally, since their protection and management has been deemed crucial for the long-term conservation of ecosystems (e.g., Büntgen, Liebhold, & Jenny, 2014). Indeed, herbivores fulfil key roles in the terrestrial trophic cascades and the maintenance of ecosystem health by affecting nutrient cycles and maintaining the diversity and stability of predators and primary producers (Bardgett & Wardle, 2010). They are also considered “environmental engineers” due to their fundamental role in the structure, composition and functioning of ecosystems (Schmitz, 2008). Numerous questions regarding the effects of global change must be answered including whether or not herbivores will be able to maintain their role in a particular ecosystem subject to change.

European mountains are a paradigmatic representation of a changing ecosystem, host of a wide variety of wild and domestic herbivores. As in other mountain ranges around the world, they have undergone a biological shift since the mid-20th century due to profound agricultural land-use and climatic changes (Mottet, Ladet, Coqué, & Gibon, 2006; Sanz-Elorza, Dana, González, & Sobrino, 2003; Steinbauer et al., 2018). The dramatic decline in rural populations and agropastoral activities have led to a general decline in livestock densities (Didier, 2001; Gartzia, Fillat, Pérez-Cabello, & Alados, 2016). Temperatures have simultaneously increased (IPCC, 2007), which have affected these ecosystems, albeit to a lesser degree, for example by stimulating shrub development or by upward shifting the tree line (Ameztegui, Coll, Brotons, & Ninot, 2016; Peñuelas, Ogaya, Boada, & S. Jump, 2007). Consequently, plant succession at varying rates leads to woody plant expansion (Mod & Luoto, 2016; Prévosto et al., 2011), resulting in a shift in dominance from herbaceous to woody plants in one of the richest habitats in the world: alpine grasslands (Wilson, Peet, Dengler, & Pärtel, 2012). However, this so-called shrubification (Martin, Jeffers, Petrokofsky, Myers-smith, & Macias-Fauria, 2017) generally decreases the diversity of plant species (Koch, Edwards, Blanckenhorn, Walter, & Hofer, 2015; Tasser & Tappeiner, 2002), the productivity of the environment (Lett & Knapp, 2003) and the diversity and total abundance of mammals (Stanton et al., 2018). Community composition and ecological interactions between species, including herbivore–plant interactions, are being importantly restructured (Lurgi, Lopez, & Montoya, 2012). These trends will likely continue as models predict a continuous increase in temperature (López-Moreno, Goyette, & Beniston, 2008) and a decrease in rural agropastoral activities (Mann, 2013; Verburg, Berkel, Doorn, Eupen, & Heiligenberg, 2010).

The Pyrenees, in southwest Europe, have experienced a major expansion and densification of shrubland and forested areas over the last century. For this reason, they constitute an ideal study case of the effects of land-use and climate change on natural communities. Not only have tree line ecotones increased on average by 35 m (Ameztegui et al., 2016), with forest cover in some areas expanding by at least two-thirds (Lasanta-Martínez, Vicente-Serrano, & Cuadrat-Prats, 2005; Poyatos, Latron, & Llorens, 2003), but they have also experienced an increase in recent summer temperatures occurring at an unprecedented rate (Büntgen, Frank, Grudd, & Esper, 2008; Büntgen, Krusic, & Verstege, 2017). These locally detected changes are consistent with a larger-scale trend across most (or even all) of the European mountain systems (Figure 1).

Figure 1.

Figure 1

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Schematic representation of the primary causes of woody plant expansion in European alpine ecosystems. The decrease in mountain rural populations causes a decline in agropastoral activities and therefore a reduction in livestock densities. At the same time, temperatures increase due to climate change. The combination of these factors leads to the expansion of woody plants in alpine grasslands (1. Gartzia et al., 2016; 2. Didier, 2001; 3. Metailié & Paegelow, 2005; 4. Lasanta-Martínez et al., 2005; 5. Collantes, 2006; 6. Sturaro, Cocca, Fuser, & Ramanzin, 2005; 7. Büntgen, Frank, Nievergelt, & Esper, 2006; 8. Büntgen et al., 2017; 9. Cannone, Sgorbati, & Guglielmin, 2007; 10. Roura-Pascual, Pons, Etienne, & Lambert, 2005; 11. Bartolomé et al., 2005; 12. Kozak, Estreguil, & Troll, 2007)

Through evolution, and in some cases further domestication, large herbivores present in the Pyrenean grasslands display a wide range of body sizes, digestive systems and feeding behaviours adapted to specific diets. They are consequently expected to respond differently to habitat change (Somero, 2010) and are thus good models for the study of species-specific effects of woody plant expansion.

The aim of this study is to explore the potential impact of the expansion of woody plant coverage on four herbivore species in the eastern Spanish Pyrenees—the wild Pyrenean chamois (Rupicapra p. pyrenaica), as well as seasonal domestic cattle, sheep and horses—that inhabit the same alpine habitats. Traditional farming is based on live-stock freely living and grazing on alpine grasslands during the summer to reduce the economic costs involved in livestock maintenance. Once the yield of these human-created grasslands decay, livestock is then moved to the hay meadows in the lower parts of the valleys until the following spring (Montserrat & Fillat, 1990). The Pyrenean chamois is a medium-sized wild caprinae well-adapted to mountain environments. They are considered mixed feeders, which consume a wide variety of resources depending on the habitat and season, following the annual cycle of primary productivity (Espunyes, Bartolomé, & Garel, 2019). Together, these four species represent a contrasting collection of energetic requirements (large- vs. medium-sized herbivores), feeding behaviours (grazers vs. mixed feeders), digestive physiologies (rumen vs. hindgut fermenters) and origins (livestock vs. wildlife).

We devised various scenarios of shrubification based on the current vegetation cover, where shrubland and woodland proliferate at the expense of grassland following models of projected woody plant expansion. We then use these shrubification scenarios and the diet composition of the ensemble of herbivores to predict how phenotypic plasticity and biotic interactions mediate the effects of shrubification. Given the diverse dietary requirements of our four species, we hypothesize that changes in land cover would affect each species differently, with grazers being more severely and rapidly affected than mixed feeders.

2. Methods

2.1. Study area

The study was carried out in the Freser-Setcases National Game Reserve (FSNGR), in the eastern part of the Spanish Pyrenees (42°22′N, 2°09′E). This area of 410 ha is known as Costabona and ranges from 1,500 to 2,400 m.a.s.l. It belongs to the sub-humid subalpine and alpine bioclimatic belts of the southern slopes of the Pyrenees, with a noticeable Mediterranean climatic influence (Vigo, 2008). Mean annual temperature for 2009–2012 was 5.7°C (daily min = –18.2, max = 26.6), and mean yearly accumulated rainfall for the same period was 1,042.4 mm (yearly min = 762.6, max = 1,282.8). These data were obtained from the Nuria meteorological station at 1,971 m.a.s.l. in the core of the FSNGR (Servei Meteorològic de Catalunya).

The vegetation cover of our study area was assessed in June 2011 following the line-intercept method proposed by Cummings and Smith (2000). The cover of all plant species present was recorded along six randomly selected transects of 10 × 0.1 m at different altitudes.

2.2. Collection and analysis of faeces

Fresh faecal samples from each of the four ungulates considered in this study (namely Pyrenean chamois, cattle, horses and sheep) were collected monthly from June to October 2011 and 2012 (except in September 2012 when sampling was not possible due to adverse meteorological conditions), coinciding with the presence of the four species in the area. Once every month, two observers walked a transect of about 5 km, covering the entire altitudinal range and main vegetation communities of the study area. Fresh faecal samples from at least five individuals per species were collected and pooled together before being transported to the laboratory and frozen at –20°C after every session. A total of nine pooled samples was obtained per species. This sampling procedure was used to obtain a general overview of the variability of feeding in the field during the three periods of plant phenology in our study area (namely: green-up, plateau greenness and senescence periods; Villamuelas, Fernández, & Albanell, 2016).

A faecal cuticle microhistological analysis was used to determine dietary composition, adapted from a protocol described by Stewart (1967). The samples were thawed, washed and ground to separate the epidermal fragments. Ten grams of sample were then placed in a test tube containing 5 ml of 65% concentrated nitric acid, boiled in a water bath for 1 min, and diluted with 200 ml of water. This suspension was passed through 1.00- and 0.25-mm filters. The 0.25–1.00 mm fraction was spread on glass microscope slides in 50% glycerol, and cover-slips were fixed with DPX micro-histological varnish. Two slides were prepared from each sample. The slides were microscopically examined by the same operator at magnifications of 100× and 400×, and 200 fragments of plant epidermis were identified per sample. An epidermis collection of the 55 main plant species in the study area were collected and used for fragment identification. Plant cuticles were identified to the species or genus level depending on the difficulty of the task.

2.3. Simulation of woody plant expansion

Patterns of expansion of woody plants into grasslands have been studied worldwide (Bartolomé, Plaixats, Fanlo, & Boada, 2005; Eldridge et al., 2011; Falcucci, Maiorano, & Boitani, 2007; Olsson, Austrheim, & Grenne, 2000). This plant succession can proceed at different speeds and with different numbers of stages depending on land-use patterns, initial state, altitude or topography (Tasser & Tappeiner, 2002; Vacquié et al., 2016). This process can nevertheless be synthesized in a first successional stage when herbaceous species are replaced by shrubs, followed by a second successional stage when shrubs are replaced by trees (Améztegui, Brotons, & Coll, 2010; Gellrich, Baur, Koch, & Zimmermann, 2007; Tasser, Walde, Tappeiner, Teutsch, & Noggler, 2007; Wallentin, Tappeiner, Strobl, & Tasser, 2008). Succession can be fast; descriptive and predictive studies have demonstrated that woody plant cover can increase by 0.5%–5% per year (Barger et al., 2011; Komac, Kefi, Nuche, Escós, & Alados, 2013).

To simulate the effects of woody plant expansion, we devised eight hypothetical scenarios where shrubland and woodland proliferate at the expense of grassland without any agricultural practices or forestry management. Based on the original vegetation availability in the study area, we designed shrubification scenarios where woody plants increased and graminoids and forbs decreased proportionally. The initial state of the system (i.e., original scenario) comprised a relative abundance of woody species of 21.4% (19.6% shrubs and 1.8% trees). Total relative abundance of woody plants was then increased by intervals of 10% per scenario until reaching 100% of woody plant cover (except the first scenario which increased by 8.6% to achieve 30% woody plant cover). This procedure yielded nine scenarios of woody plant cover (the original scenario plus eight hypothetical): 21.4%, 30%, 40%, 50%, 60%, 70%, 80%, 90% and 100%, respectively. The increase in woody plant cover was distributed proportionally across the plant species included in this category according to their relative abundance. For example, if woody plant cover increased by 20% and the plant Juniperus communis represents 50% of the total woody plant cover then a 10% increase of that plant was simulated. Conversely, the cover of forbs and graminoids was decreased by the same fraction of woody plant increase. This decrease was also distributed proportionally between the species of these categories (see Table S1).

2.4. Landscape-use efficiency

The breadth of a resource niche can be used as a proxy for species performance (Rotenberry & Wiens, 1980) or to quantify the extent to which organisms are able to exploit their environment (Krebs, 1999). We used the measure of niche breadth proposed by Smith (1982) as a proxy for the efficiency in the use of resources by the herbivores (i.e., landscape-use efficiency, LUE).

LUE for each herbivore in each shrubification scenario was calculated as:

LUE=Σ(Pj×Aj)

where Pj is the proportion of plant j in the diet of the herbivore, and Aj is the proportion of plant j available in the study area. This index ranges from nearly zero, for the narrowest possible niche when a species is specialized in eating the rarest resources, to one, for the broadest possible niche when a species uses resources in proportion to their availability. This index is thus low when a species inefficiently uses the resources of its habitat and is high when a species uses them efficiently (i.e., proportionally to the availability).

2.5. Statistical analysis

After describing the diets of our studied species by basic statistics, we performed a nonparametric multivariate analysis of similarity (ANOSIM; Clarke, 1993) to check for differences in diets between herbivores. The ANOSIM statistic R is based on the difference of mean ranks between groups and within groups and a high value of R in this analysis indicates a high dissimilarity between groups. A nonmetric multidimensional scaling (NMDS) plot based on Bray–Curtis dissimilarity indices was created to visually identify the patterns in dietary similarities between species. Stress, a measure of goodness of fit should be <0.2 in order to have a good representation with no prospect of misinterpretation (Clarke & Warwick, 2001). Our NMDS stress was 0.0985 so our representation was considered to be sufficiently well-described in two dimensions. The ANOSIM and the NMDS plot were performed using the R vegan package (version 2.4-5, Oksanen, Blanchet, & Friendly, 2017).

We then evaluated the impact of woody plant expansion (i.e., woody plant abundance in the scenarios) on the LUE of each species by a linear model (LM). LUE of each species was the response variable in our LM whereas the interaction between animal species and degree of woody plant expansion were our fixed explanatory factors. Interspecific differences of LUE values were analysed with a pairwise Mann–Whitney U test using the FSA package (version 0.8.17, Ogle, 2017).

Normality of residuals and homogeneity of variance assumptions were checked previous to the performance of any analysis. All statistical analyses were performed using R version 3.4.3 (R Core Team, 2018).

3. Results

3.1. Initial state of the system and herbivore diets

We recorded 65 plant species in our study area. Graminoids represented half of the vegetation cover (51.6%), where Festuca spp. was clearly dominant (32.3%), followed by Carex cariophyllea (12.4%). Forbs covered almost one-third of the area and were dominated by Trifolium alpinum (7.5%), followed by Trifolium repens (1.5%) and Hippocrepis comosa (1.4%). The other plants were woody species (shrubs and trees, 21.2%), where dwarf shrubs (Calluna vulgaris and Juniperus communis) and legumes Cytisus spp. were the most common (see Table S1).

The ANOSIM indicated that the differences in dietary composition were higher between Pyrenean chamois and the livestock than amongst the livestock species (Table 1). Among the livestock diets, horse diet differed the most from the rest, while cattle and sheep showed more similar dietary compositions. The NMDS plot supported these interspecific dietary differences (Figure 2).

Table 1. Differences in dietary composition between alpine ungulates in the Pyrenees.

Cattle Horses Sheep
Chamois R = 0.506
p = 0.002		 R = 0.692
p = 0.001		 R = 0.569
p = 0.001
Sheep R = 0.246
p = 0.013		 R = 0.692
p = 0.001		 R = 0.427
p = 0.001
Horses R = 0.386
p = 0.002
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Notes. Summary of the pairwise ANOSIM of the differences in dietary composition between Pyrenean chamois, cattle, horses and sheep from June to October 2011 and 2012 in the eastern Spanish Pyrenees. A high value of R in this analysis indicates a high dissimilarity between groups.

Figure 2.

Figure 2

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Diet dissimilarity among alpine ungulates in the Pyrenees. Nonmetric multidimensional scaling (NMDS) plot representing dietary dissimilarity for seasonal livestock (cattle, horses and sheep) and Pyrenean chamois from June to October 2011 and 2012 in eastern Spanish Pyrenees. When stress, a measure of goodness of fit, is <0.2, NMDS reproduces an adequate depiction of the groups

Analysis of diet composition for livestock during summer and autumn showed a larger overall content of graminoid and forb fragments compared to woody plants. Horses were the most extreme livestock species with the highest consumption of graminoids (63.7%) and the lowest consumption of woody plants (5.9%; see Table 2). On the contrary, Pyrenean chamois faeces had the highest content of woody plant fragments (48.6%) and the lowest content of graminoids (25.8%) and forbs (25.3%). Cattle and sheep had similar diets (R = 0.246, see Table 1), but cattle showed a higher content of graminoids (cattle: 49.8%; sheep: 45.9%) and woody plants (cattle: 16.2%; sheep: 12.4%) and a lower content of forbs (Cattle: 34.1%; sheep: 41.6%).

Table 2. Dietary composition of Pyrenean chamois and seasonal cattle, horses and sheep in the Pyrenees.

Chamois Cattle Horses Sheep
Woody plants
   Calluna vulgaris     24.6 (0.0–6.0)     10.9 (1.0–22.5)     2.2 (0.0–12.0)     2.1 (0.0–29.5)
   Cytisus spp.     17.3 (3.5–51.5)       0.1 (0.0–0.5)     0.0 (0.0–0.0)     0.3 (0.0–6.0)
   Other woody plants       7.1 (0.0–17.5)       5.2 (2.0–8)     3.7 (0.5–9.5)   10.1 (3.0–17.0)
   Total     48.6     16.2     5.9   12.4
Graminoids
    Festuca spp.     22.0 (8.5–50.0)     40.4 (26.5–52.0)   52.4 (43.0–63.5)   40.4 (27.5–52.0)
    Avenula pratensis       1.8 (0.0–6.5)       3.2 (0.0–6.5)     1.8 (0.0–6.0)     2.1 (0.0–4.5)
    Other graminoids       2.1 (0.0–6.5)       6.2 (3.0–11.5)     9.5 (5.0–13.0)     3.4 (2.0–7.0)
    Total     25.8     49.8   63.7   45.9
Forbs
    Anthyllis vulneraria       1.3 (0.0–5.0)       2.2 (0.0–7.0)     1.5 (0.0–4.5)     4.1 (2.0–6.5)
    Plantago monosperma       3.6 (0.0–9.0)       3.5 (2.0–5.0)     3.9 (2.0–8.0)     5.2 (3.0–10.0)
    Potentilla spp.       2.5 (0.0–6.0)       3.9 (2.0–6.0)     2.2 (0.5–4.5)     4.7 (1.5–8.0)
    Trifolium spp.     11.2 (2.0–17.5)     13.4 (5.5–21.0)   13.8 (7.0–20.0)   14.2 (6.0–21.5)
    Other forbs       6.7 (2.5–10.5)     10.9 (4.0–17.0)     9.1 (5.0–19.0)   13.5 (8.5–20.0)
    Total     25.3     34.1   30.4   41.6
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Notes. Data from June to October 2011 and 2012 in the Freser-Setcases National Game Reserve (eastern Spanish Pyrenees). Values represent mean percentages of fragment frequency (min–max).

3.2. Simulation of woody plant expansion and LUE

Changes in LUE through the hypothetical scenarios of woody plant expansion suggested that horses would be most affected by the disappearance of grasslands in the Pyrenees. Pyrenean chamois, on the other hand, could even benefit during the early stages of expansion (Figure 3). Current LUE is lower for chamois (median=0.72, min = 0.57, max = 0.75) than livestock (cattle: median=0.76, min = 0.70, max = 0.79; horses: median=0.74, min = 0.71, max = 0.79; sheep: median=0.73, min = 0.69, max = 0.77; significantly different only between cattle and chamois, w = 73, p = 0.0028). Our LM revealed that 76.8% of the observed LUE variability was explained by the interaction between woody plant expansion and ungulate species (F3,316 = 149.2, p < 0.001).

Figure 3.

Figure 3

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Evolution of the landscape-use efficiencies (LUE) of Pyrenean chamois and seasonal livestock along different scenarios of woody plant expansion. Slopes of the linear regression are also reported for each species

The LUE of all the herbivores studied decreased to some degree from the initial to the final scenario (Figure 3). However, this decrease was sharper in livestock species. In fact, the LUE of chamois remained practically stable until woody plant cover reached 90%. It even increased slightly in scenarios of initial shrubification and then began to decrease moderately from the fourth hypothetical scenario (60% woody plant abundance) onwards, acquiring at the same time the highest values relative to the other species. Livestock, however, lost their foraging resilience at very early degrees of shrubification (Figure 3). The LUE of cattle (β = –0.005, SE = 0.0005, p < 0.001), sheep (β = –0.004, SE = 0.0005, p < 0.001) and horses (β = –0.005, SE = 0.0005, p < 0.001), steadily decreased from the first scenario of shrubification. The LUE of sheep and horses were significantly smaller than chamois from the third hypothetical scenario onwards (50% woody plant cover; w = 74, p < 0.005 and w = 75, p < 0.005, respectively) and cattle differed from the fourth scenario onwards (60% woody plant cover; w = 14, p < 0.05).

The lowest LUE values were detected in our final scenario of shrubification, where woody plants occupied the entire area, notably decreasing livestock LUE (cattle: median=0.29, min = 0.14, max = 0.41; sheep: median=0.17, min = 0.06, max = 0.29; horses: median=0.09, min = 0.14, max = 0.29). LUE was significantly higher for chamois (median=0.56, min = 0.21, max = 0.70) than cattle (w = 13, p = 0.014), sheep (w = 76, p < 0.0001) and horses (w = 79, p < 0.001) due to its moderate decrease in niche breadth along the scenarios. Livestock LUEs differed significantly only between cattle and horses (w = 71, p = 0.006).

4. Discussion

Our results suggest that woody plant expansion in an unmanaged environment will affect herbivores in alpine grasslands during summer and autumn but that the magnitudes and direction of these effects will vary between species. Animals with a preference for herbaceous plants will have difficulties to follow the same diet and they will need to acclimatize to a higher consumption of woody plants in order to remain in these areas. At the same time, competition for the most consumed plants, such as Festuca spp. or Trifolium spp., would lead to overgrazing, one of the main causes of rangeland degradation worldwide (Du Toit, Kock, & Deutsch, 2010; Hilker, Natsagdorj, Waring, Lyapustin, & Wang, 2014).

Changes in woody plant cover importantly restructure the wild herbivore assemblage as grazer densities decrease when woody cover increases (Smit & Prins, 2015). The increasing woody plant expansion in alpine environments will render grazers less efficient users of their landscape, as our predictions suggested, therefore decreasing their density in response to food availability. Livestock are highly dependent on the availability of montane grasslands, and the number of livestock grazers will have to decrease to prevent a reduction in productivity. In fact, increases in woody plant cover are already having repercussions on livestock production and reproduction (Anadon, Sala, Turner, & Bennett, 2014). The need to maintain sustainable levels of production will force farmers to move livestock to more suitable areas. Habitat diversity will consequently decline even faster in alpine areas, because plant species richness is maintained by grazing in these human-created herbaceous communities (Bakker, 1998; Boulanger, Dupouey, & Archaux, 2018).

Horses feed mostly on graminoids and, to a lesser extent, on forbs and thus would be more quickly and broadly affected by woody plant expansion. This strong dependence on herbaceous plants has been widely described in feral and free-ranging horses (Celaya, Ferreira, García, Duncan, 1992; Rosa García, & Osoro, 2011; Olsen & Hansen, 1977; Salter & Hudson, 1979). The consumption of grasses (50% of total consumption) can be lower in some extreme environments, such as the Chihuahuan Desert (Hansen, 1976), but animal growth is usually restricted when high-quality pastures are not readily available (Andreyev, 1971; Celaya et al., 2011; Dawson, Phillips, & Speelman, 1945). The production of horse meat in the Pyrenees, as in other parts of Europe, is exclusively free-range. Animals make use of grasslands at different altitudes according to the season and, as a consequence, depend highly on montane pastures to subsist (Martin-Rosset & Trillaud-Geyl, 2015). Woody plant expansion is therefore a real threat to horse meat production.

Our results support those of several studies that found that free-ranging cattle generally consume higher proportions of forbs and woody plants than horses (Celaya et al., 2011; Krysl et al., 1984; Menard, Duncan, Fleurance, Georges, & Lila, 2002; Scasta, Beck, & Angwin, 2016). Woody plant expansion would thus affect cattle less than horses. Diets can be more variable and contain more woody species in free-ranging cattle than horses, although diets of cattle can also be high in graminoids and forbs (Aldezabal, García-González, Gómez, & Fillat, 2002; Scasta et al., 2016). The high content of plant secondary metabolites in shrubs, such as tannins, can affect intake, digestion and metabolism in herbivores and can be toxic if consumed in large amounts (Burrit & Provenza, 2000; Hanley, Robbins, Hagerman, & McArthur, 1992). Cattle can consume a relatively high proportion of woody plants in specific habitats and conditions, but this rusticity and adaptability are only observed in some local breeds (Bartolomé, Plaixats, & Piedrafita, 2011; Guevara, 1996). However, local breeds have been gradually abandoned in recent decades for the benefit of highly productive commercial breeds (Taberlet et al., 2008) and consequently, many locally adapted breeds have already become extinct (Scherf, 2000). At the same time, the use of these breeds is impaired by important inbreeding situations and small effective population sizes (Taberlet et al., 2008), highlighting future challenges of livestock farming in areas were local adaptations will be needed.

Medium-sized herbivores, such as sheep, tend to have a proportionally higher maintenance cost per body weight unit (Kleiber, 1961). They therefore need to forage on plants higher in nutritional value compared to larger herbivores, such as cattle or horses. Sheep can select preferred components in fine-scale mixtures due to their smaller size, which determines gape size, and can therefore feed on the more nutritional parts of plants (Gordon & Illius, 1988). Studies on the composition of diets have reported higher contents of forbs and woody plants by sheep than by large herbivores (Karmiris & Nastis, 2010; La Morgia & Bassano, 2009). Still, the consumption of graminoids and forbs by sheep and cattle in our study was similar, probably due to the high availability of these resources in our study area, generating a strong overlap in the use of resources.

The societal demand for livestock products is increasing the development of research programmes focusing on animal behaviour and genetics for developing animals able to use shrubs more efficiently (Estell et al., 2012). The productivity of these breeds, however, is currently relatively low (Verrier, Tixier-Boichard, Bernigaud, & Naves, 2005), and animals in mountainous areas have adaptations and functional traits of interest for the montane farming system but a lower production of muscle or milk than commercial breeds (Verrier et al., 2005). The use of shrub-dominated areas for meat or milk production does not presently meet animal requirements (Casasús, Bernués, Sanz, Riedel, & Revilla, 2005). These practices appear unsustainable due to the necessity of management intervention (e.g., thinning and spraying) and intensive supplementary feeding (Brosh, Henkin, Orlov, & Aharoni, 2006; Gutman, Henkin, Holzer, Noy-Meir, & Seligman, 2000). As a consequence, livestock farming in areas suffering from woody plant expansion will be at high economic risk due to the impossibility of maintaining sustained economic incomes.

Livestock farming in mountainous areas is important to local economies and cultural heritages and is often essential for the livelihood of rural populations worldwide (Mann, 2013). In fact, 32% of Kenyans inhabiting mountains mainly depend on livestock farming to subsist and in Nepalese mountains, where 59% of the population lives below the poverty line, livestock contribute to 21.2% of total household incomes (Abington, 1992; Golicha, Ngutu, & Charfi, 2012). Besides a direct nutritional income through meat or milk, livestock also play a vital role in supporting farming systems providing wool, manure, working traction, transportation, cash income and risk diversification (Sherman, 2005). In rural areas where subsistence agriculture is prevalent, the loss of pasture land would have a dramatic socio-economic impact, regardless of the causes of the local shrubification.

We found that Pyrenean chamois during summer and autumn would be favoured by a moderate to high expansion of woody plants due to their ability to balance their feeding behaviour between grazing and browsing. In fact, chamois can have extremely diverse dietary preferences depending on the habitat and season (Herrero, Garin, García-Serrano, & García-González, 1996; La Morgia & Bassano, 2009) and can even be exclusively dependent on woody species (Yockney & Hickling, 2000). This high phenotypical plasticity is due to their capacity to alternate between ruminal and hindgut fermentation depending on forage quantity and quality (Hofmann, 1989). Because chamois evolved during thousands of years in unmanaged environments (Masini & Lovari, 1988) it is not surprising that the reversion to unmanaged conditions could favour them. The chamois diet in our study area differed from the diets of all the livestock species and showed an evenly distributed consumption of herbaceous and woody plants, despite a lower availability of the latter. This behaviour will allow the chamois to have a higher theoretical LUE than the other herbivores in scenarios of future woody plant expansion. Furthermore, mixed feeders may even be able to slow shrub expansion (Olofsson et al., 2009; Schulze, Rosenthal, & Peringer, 2018), highlighting the importance of the conservation of these herbivores to maintain open habitats. Our results suggest that the LUE of chamois would be impaired in scenarios of extreme shrubification, despite their adaptation to a high consumption of woody plants. However, the phenotypic capacity of chamois could allow them to consume more woody plants than observed in our study area but further studies would be necessary to assess the effect of these dietary adaptations on the performance of this species. At the same time, this study focussed on summer and autumn diets of chamois because there are key for the reproduction and survival of the species (Garel et al., 2011; Scornavacca et al., 2016). Food availability during winter may also determine chamois survival, but there is no information on that process. Hence, further investigations will be required to determine the impact of shrubification on the survival of chamois during winter.

Our data also suggest that extensive land management and human intervention (e.g. manual shrub clearance), will be necessary for maintaining semi-natural grasslands and free-range farming systems. Keeping in mind that half of the European network of Natura 2000 sites are associated with farming, agricultural land abandonment may have important impacts on landscape and biodiversity in Europe (MacDonald, Crabtree, & Wiesinger, 2000). Moreover, in a kind of vicious circle, the capital investment needed and the time and effort of the demanding work to reverse woody plant expansion on agricultural land is leading to an intensification of the abandonment of farmland and rural areas, accelerating shrubification (MacDonald et al., 2000). Being a driver of woody plant expansion, temperature increase in mountainous environments will also impair biodiversity and efforts to limit global warming will be capital for the future of these environments (Steffen et al., 2018).

Finally, the consequences of our results are not only representative of a Pyrenean scenario or a European montane ecosystem. Considering that shrubification is a global issue affecting other habitats and ecosystems worldwide, from the African savannah to the arctic tundra (Naito & Cairns, 2011; Tape, Sturm, & Racine, 2006), lessons learned from this paradigmatic case example can be extrapolated to a global scale.

Supplementary Material

Additional supporting information may be found online in the Supporting Information section at the end of the article.

Supplementary Table

Acknowledgements

We thank the National Game Reserve of Freser-Setcases personnel for their authorization to carry out this study. We also thank Marco Apollonio and an anonymous reviewer for valuable feedback on the early draft of this manuscript. JE acknowledges a pre-doctoral grant from the Government of Andorra, ATC015 - AND - 2015/2016, 2016/2017 and 2017/2018. ML is supported by the French ANR through LabEx TULIP (ANR-10-LABX-41; ANR-11-IDEX-002-02), by the Midi-Pyrénées region (grant number CNRS 121090), and by the FRAGCLIM Consolidator Grant, funded by the European Research Council under the European Union's Horizon 2020 research and innovation programme (grant agreement number 726176). ES was funded by the Spanish Ministerio de Economia y Competitividad (MINECO) through a Ramon y Cajal agreement (RYC-2016-21120).

Funding information

French ANR, Grant/Award Number: ANR-10-LABX-41 and ANR-11-IDEX-002-02; Midi-Pyrénées region, Grant/Award Number: CNRS 121090; European Research Council; Horizon 2020, Grant/Award Number: 726176; Spanish Ministerio de Economia y Competitividad (MINECO), Grant/Award Number: RYC-2016-2112

Orcid

References

  1. Abington JB, editor. Sustainable Livestock Production in the Mountain Agro-ecosystem of Nepal. Rome, Italy: Food and Agriculture Organization of the United States; 1992. [Google Scholar]
  2. Aldezabal A, García-González R, Gómez D, Fillat F. El papel de los herbívoros en la conservación de los pastos. Ecosistemas. 2002;11 [Google Scholar]
  3. Améztegui A, Brotons L, Coll L. Land-use changes as major drivers of mountain pine (Pinus uncinata Ram.) expansion in the Pyrenees. Global Ecology and Biogeography. 2010;19:632–641. doi: 10.1111/j.1466-8238.2010.00550.x. [DOI] [Google Scholar]
  4. Ameztegui A, Coll L, Brotons L, Ninot JM. Land-use legacies rather than climate change are driving the recent upward shift of the mountain tree line in the Pyrenees. Global Ecology and Biogeography. 2016;25:263–273. doi: 10.1111/geb.12407. [DOI] [Google Scholar]
  5. Anadon JD, Sala OE, Turner BL, Bennett EM. Effect of woody-plant encroachment on livestock production in North and South America. Proceedings of the National Academy of Sciences. 2014;111:12948–12953. doi: 10.1073/pnas.1320585111. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Andreyev VN. Horse herding for meat in Yakutskaya ASSR. Polar Record. 1971;15:931–933. doi: 10.1017/S0032247400062197. [DOI] [Google Scholar]
  7. Bakker JP. The impact of grazing to plant communities. In: Wallis de Vries MF, Bakker JP, Van Wieren SE, editors. Grazing and conservation management. Dordrecht: Kluwer Academic Publishers; 1998. pp. 137–184. [Google Scholar]
  8. Bardgett RD, Wardle DA. Aboveground– Belowground Linkages. Biotic Interactions: Ecosystem Processes, and Global Change. Oxford University Press; 2010. p. 312. [Google Scholar]
  9. Barger NN, Archer SR, Campbell JL, Huang C, Morton JA, Knapp AK. Woody plant proliferation in North American drylands: A synthesis of impacts on ecosystem carbon balance. Journal of Geophysical Research. 2011;116 doi: 10.1029/2010JG001506. [DOI] [Google Scholar]
  10. Bartolomé J, Plaixats J, Fanlo R, Boada M. Conservation of isolated Atlantic heathlands in the Mediterranean region: Effects of land-use changes in the Montseny biosphere reserve (Spain) Biological Conservation. 2005;122:81–88. doi: 10.1016/j.biocon.2004.05.024. [DOI] [Google Scholar]
  11. Bartolomé J, Plaixats J, Piedrafita J, Fina M, Adrobau E, Aixàs A, et al. Polo L. Foraging Behavior of Alberes Cattle in a Mediterranean Forest Ecosystem. Rangeland Ecology & Management. 2011;64:319–324. doi: 10.2111/REM-D-09-00160.1. [DOI] [Google Scholar]
  12. Boulanger V, Dupouey JL, Archaux F, Badeau V, Baltzinger C, Chevalier R, et al. Ulrich E. Ungulates increase forest plant species richness to the benefit of non-forest specialists. Global Change Biology. 2018;24:e485–e495. doi: 10.1111/gcb.13899. [DOI] [PubMed] [Google Scholar]
  13. Brosh A, Henkin Z, Orlov A, Aharoni Y. Diet composition and energy balance of cows grazing on Mediterranean woodland. Livestock Science. 2006;102:11–22. doi: 10.1016/j.livprodsci.2005.11.016. [DOI] [Google Scholar]
  14. Büntgen U, Frank D, Grudd H, Esper J. Long-term summer temperature variations in the Pyrenees. Climate Dynamics. 2008;31:615–631. doi: 10.1007/s00382-008-0390-x. [DOI] [Google Scholar]
  15. Büntgen U, Frank DC, Nievergelt D, Esper J. Summer temperature variations in the European Alps, A.D. 755–2004. Journal of Climate. 2006;19:5606–5623. [Google Scholar]
  16. Büntgen U, Krusic PJ, Verstege A, Sangüesa-Barreda G, Wagner S, Camarero J, et al. Esper J. New Tree-Ring Evidence from the Pyrenees Reveals Western Mediterranean Climate Variability since Medieval Times. Journal of Climate. 2017;30:5295–5318. doi: 10.1175/JCLI-D-16-0526.1. [DOI] [Google Scholar]
  17. Büntgen U, Liebhold A, Jenny H, Mysterud A, Egli S, Nievergelt D, et al. Bollmann K. European springtime temperature synchronises ibex horn growth across the eastern Swiss Alps. Gaillard J-M, editor. Ecology Letters. 2014;17:303–313. doi: 10.1111/ele.12231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Burrit EA, Provenza FD. The role of toxins in varied intake by sheep. Journal of Chemical Ecology. 2000;26:1991–2005. doi: 10.1023/A:1005565228064. [DOI] [Google Scholar]
  19. Cannone N, Sgorbati S, Guglielmin M. Unexpected impacts of climate change on alpine vegetation. Frontiers in Ecology and the Environment. 2007;5:360–364. doi: 10.1890/1540-9295(2007)5[360:UIOCCO]2.0.CO;2. [DOI] [Google Scholar]
  20. Casasús I, Bernués A, Sanz A, Riedel JL, Revilla R. Utilization of Mediterranean forest pastures by suckler cows: Animal performance and impact on vegetation dynamics. In: Georgoudis A, Rosati A, Mosconi C, editors. Animal production and natural resources utilisation in the Mediterranean mountain areas. Wageningen: Academic Publishers; 2005. pp. 82–88. [Google Scholar]
  21. Celaya R, Ferreira LMM, García U, Rosa García R, Osoro K. Diet selection and performance of cattle and horses grazing in heathlands. Animal. 2011;5:1467–1473. doi: 10.1017/S1751731111000449. [DOI] [PubMed] [Google Scholar]
  22. Charmantier A, McCleery RH, Cole LR, Perrins C, Kruuk LEB, Sheldon BC. Adaptive phenotypic plasticity in response to climate change in a wild bird population. Science. 2008;320:800–803. doi: 10.1126/science.1157174. [DOI] [PubMed] [Google Scholar]
  23. Clarke KR. Non-parametric multivariate analyses of changes in community structure. Austral Ecology. 1993;18:117–143. doi: 10.1111/j.1442-9993.1993.tb00438.x. [DOI] [Google Scholar]
  24. Clarke KR, Warwick RM. Change in marine communities: An approach to statistical analysis and interpretation. 2nd ed. Plymouth: PRIMER-E; 2001. [Google Scholar]
  25. Collantes F. Farewell to the peasant republic: Marginal rural communities and European industrialisation, 1815–1990. Agricultural History Review. 2006;54:257–273. [Google Scholar]
  26. Cummings J, Smith D. The line-intercept method: A tool for introductory plant ecology laboratories. In: Karcher SL, editor. Tested studies for laboratory teaching. Vol. 22. Clemson, SC: Association for Biology Laboratory Education (ABLE), Clemson University; 2000. pp. 234–246. [Google Scholar]
  27. Dawson WM, Phillips RW, Speelman SR. Growth of horses under western range conditions. Journal of Animal Science. 1945;4:47–54. doi: 10.2527/jas1945.4147. [DOI] [Google Scholar]
  28. Didier L. Invasion patterns of European larch and Swiss stone pine in subalpine pastures in the French Alps. Forest Ecology and Management. 2001;145:67–77. doi: 10.1016/S0378-1127(00)00575-2. [DOI] [Google Scholar]
  29. Du Toit JT, Kock R, Deutsch JD, editors. Wild rangelands. Oxford, UK: Wiley-Blackwell; 2010. p. 424. [Google Scholar]
  30. Duncan P. Diets – Their botanical composition and nutritional value. In: Duncan P, editor. Horses and grasses. The nutritional ecology of equids and their impact on the camargue. New York, NY: Springer-Verlag; 1992. pp. 75–97. [Google Scholar]
  31. Eldridge DJ, Bowker MA, Maestre FT, Roger E, Reynolds JF, Whitford WG. Impacts of shrub encroachment on ecosystem structure and functioning: Towards a global synthesis. Ecology Letters. 2011;14:709–722. doi: 10.1111/j.1461-0248.2011.01630.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Espunyes J, Bartolomé J, Garel M, Gálvez-Cerón A, Fernández Aguilar X, Colom-Cadena A, et al. Serrano E. Seasonal diet composition of Pyrenean chamois is mainly shaped by primary production waves. PLoS ONE. 2019;14:e0210819. doi: 10.1371/journal.pone.0210819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Estell RE, Havstad KM, Cibils AF, Fredrickson EL, Anderson DM, Schrader TS, James DK. Increasing shrub use by livestock in a world with less grass. Rangeland Ecology & Management. 2012;65:553–562. doi: 10.2111/REM-D-11-00124.1. [DOI] [Google Scholar]
  34. Falcucci A, Maiorano L, Boitani L. Changes in land-use/land-cover patterns in Italy and their implications for biodiversity conservation. Landscape Ecology. 2007;22:617–631. doi: 10.1007/s10980-006-9056-4. [DOI] [Google Scholar]
  35. Garel M, Gaillard J-M, Jullien J-M, Dubray D, Maillard D, Loison A. Population abundance and early spring conditions determine variation in body mass of juvenile chamois. Journal of Mammalogy. 2011;92:1112–1117. doi: 10.1644/10-MAMM-A-056.1. [DOI] [Google Scholar]
  36. Gartzia M, Fillat F, Pérez-Cabello F, Alados CL. Influence of agropastoral system components on mountain grassland vulnerability estimated by connectivity loss. PLoS ONE. 2016;11:1–21. doi: 10.1371/journal.pone.0155193. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Gellrich M, Baur P, Koch B, Zimmermann NE. Agricultural land abandonment and natural forest re-growth in the Swiss mountains: A spatially explicit economic analysis. Agriculture, Ecosystems and Environment. 2007;118:93–108. doi: 10.1016/j.agee.2006.05.001. [DOI] [Google Scholar]
  38. Golicha D, Ngutu M, Charfi H. Livelihood diversification options for pastoralists in mountain and oasis areas of northern Kenya. Livestock Research for Rural Development. 2012;24 [Google Scholar]
  39. Gordon IJ, Illius AW. Incisor arcade structure and diet selection in ruminants. Functional Ecology. 1988;2:15–22. doi: 10.2307/2389455. [DOI] [Google Scholar]
  40. Guevara JC. Botanical composition of the seasonal diet of cattle in the rangelands of the Monte Desert of Mendoza, Argentina. Journal of Arid Environments. 1996;32:387–394. doi: 10.1006/jare.1996.0032. [DOI] [Google Scholar]
  41. Gutman M, Henkin Z, Holzer Z, Noy-Meir I, Seligman NG. A case study of beef-cattle grazing in a Mediterranean-type woodland. Agroforestry Systems. 2000;48:119–140. [Google Scholar]
  42. Hanley TA, Robbins CT, Hagerman AE, McArthur C. Predicting digestible protein and digestible dry matter in tannin-containing forages consumed by ruminants. Ecology. 1992;73:537–541. doi: 10.2307/1940759. [DOI] [Google Scholar]
  43. Hansen RM. Foods of free-roaming horses in Southern New Mexico. Journal of Range Management. 1976;29:347. doi: 10.2307/3897105. [DOI] [Google Scholar]
  44. Herrero J, Garin I, García-Serrano A, García-González R. Habitat use in a Rupicapra pyrenaica pyrenaica forest population. Forest Ecology and Management. 1996;88:25–29. doi: 10.1016/S0378-1127(96)038066. [DOI] [Google Scholar]
  45. Hilker T, Natsagdorj E, Waring RH, Lyapustin A, Wang Y. Satellite observed widespread decline in Mongolian grasslands largely due to overgrazing. Global Change Biology. 2014;20:418–428. doi: 10.1111/gcb.12365. [DOI] [PubMed] [Google Scholar]
  46. Hofmann RR. Evolutionary steps of ecophysiological adaptation and diversification of ruminants: A comparative view of their digestive system. Oecologia. 1989;78:443–457. doi: 10.1007/BF00378733. [DOI] [PubMed] [Google Scholar]
  47. IPCC. Climate change 2007: Impacts, adaptation and vulnerability. In: Parry M, Canziani O, Palutikof J, van derLinden P, Hanson C, editors. Contribution of working group II to the fourth assessment report of the intergovernmental panel on climate change. Cambridge, UK: Cambridge University Press; 2007. p. 976. [Google Scholar]
  48. Karmiris I, Nastis A. Diet overlap between small ruminants and the European hare in a Mediterranean shrubland. Open Life Sciences. 2010;5:729–737. doi: 10.2478/s11535-010-0056-7. [DOI] [Google Scholar]
  49. Kleiber M. The fire of life. An introduction to animal energetics. New York, NY, Englewood Cliffs, NJ, USA: John Wiley; 1961. p. 454. [Google Scholar]
  50. Koch B, Edwards PJ, Blanckenhorn WU, Walter T, Hofer G. Shrub encroachment affects the diversity of plants, butterflies, and grasshoppers on two Swiss subalpine pastures. Arctic, Antarctic, and Alpine Research. 2015;47:345–357. doi: 10.1657/AAAR0013-093. [DOI] [Google Scholar]
  51. Komac B, Kefi S, Nuche P, Escós J, Alados CL. Modeling shrub encroachment in subalpine grasslands under different environmental and management scenarios. Journal of Environmental Management. 2013;121:160–169. doi: 10.1016/j.jenvman.2013.01.038. [DOI] [PubMed] [Google Scholar]
  52. Kozak J, Estreguil C, Troll M. Forest cover changes in the northern Carpathians in the 20th century: A slow transition. Journal of Land Use Science. 2007;2:127–146. doi: 10.1080/17474230701218244. [DOI] [Google Scholar]
  53. Krebs CJ. Ecological methodology. Menlo Park, CA: Benjamin/Cummings; 1999. p. 620. [Google Scholar]
  54. Krysl LJ, Hubbert ME, Sowell BF, Plumb GE, Jewett TK, Smith MA, Waggoner JW. Horses and cattle grazing in the Wyoming Red Desert, I. Food habits and dietary overlap. Journal of Range Management. 1984;37:72–76. doi: 10.2307/3898828. [DOI] [Google Scholar]
  55. La Morgia V, Bassano B. Feeding habits, forage selection, and diet overlap in Alpine chamois (Rupicapra rupicapra L.) and domestic sheep. Ecological Research. 2009;24:1043–1050. doi: 10.1007/s11284-008-0581-2. [DOI] [Google Scholar]
  56. Lasanta-Martínez T, Vicente-Serrano SM, Cuadrat-Prats JM. Mountain Mediterranean landscape evolution caused by the abandonment of traditional primary activities: A study of the Spanish Central Pyrenees. Applied Geography. 2005;25:47–65. doi: 10.1016/j.apgeog.2004.11.001. [DOI] [Google Scholar]
  57. Lett MS, Knapp AK. Consequences of shrub expansion in mesic grassland: Resource alterations and graminoid responses. Journal of Vegetation Science. 2003;14:487–496. doi: 10.1111/j.1654-1103.2003.tb02175.x. [DOI] [Google Scholar]
  58. Loarie SR, Duffy PB, Hamilton H, Asner GP, Field CB, Ackerly DD. The velocity of climate change. Nature. 2009;462:1052–1055. doi: 10.1038/nature08649. [DOI] [PubMed] [Google Scholar]
  59. López-Moreno JI, Goyette S, Beniston M. Climate change prediction over complex areas: Spatial variability of uncertainties and predictions over the Pyrenees from a set of regional climate models. International Journal of Climatology. 2008;28:1535–1550. doi: 10.1002/joc.1645. [DOI] [Google Scholar]
  60. Lurgi M, Lopez BC, Montoya JM. Climate change impacts on body size and food web structure on mountain ecosystems. Philosophical Transactions of the Royal Society B: Biological Sciences. 2012;367:3050–3057. doi: 10.1098/rstb.2012.0239. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. MacDonald D, Crabtree J, Wiesinger G, Dax T, Stamou N, Fleury P, et al. Gibon A. Agricultural abandonment in mountain areas of Europe: Environmental consequences and policy response. Journal of Environmental Management. 2000;59:47–69. doi: 10.1006/jema.1999.0335. [DOI] [Google Scholar]
  62. Mann S, editor. The future of mountain agriculture. Berlin, Heidelberg: Springer Berlin Heidelberg; 2013. p. 176. [Google Scholar]
  63. Martin AC, Jeffers ES, Petrokofsky G, Myers-smith I, Macias-Fauria M. Shrub growth and expansion in the Arctic tundra : An assessment of controlling factors using an evidence-based approach. Environmental Research Letters. 2017;12:085007. doi: 10.1088/1748-9326/aa7989. [DOI] [Google Scholar]
  64. Martin-Rosset W, Trillaud-Geyl C. Horse meat production and characteristics: A review. In: Vial C, Evans R, editors. The new equine economy in the 21st century. Wageningen: Academic Publishers; 2015. pp. 197–222. EAAP Scientific Series publication no136. [Google Scholar]
  65. Masini F, Lovari S. Systematics, phylogenetic relationships, and dispersal of the chamois (Rupicapra spp.) Quaternary Research. 1988;30:339–349. doi: 10.1016/0033-5894(88)90009-9. [DOI] [Google Scholar]
  66. Menard C, Duncan P, Fleurance G, Georges JY, Lila M. Comparative foraging and nutrition of horses and cattle in European wetlands. Journal of Applied Ecology. 2002;39:120–133. doi: 10.1046/j.1365-2664.2002.00693.x. [DOI] [Google Scholar]
  67. Metailié JP, Paegelow M. Land abandonment and the spreading of the forest in the Eastern French Pyrenées in the nineteenth to twentieth centuries. In: Mazzoleni S, Di Pasquale G, Mulligan M, Di Martino P, Rego F, editors. Recent dynamics of the Mediterranean vegetation and landscape. Chichester, UK: John Wiley; 2005. pp. 217–236. [Google Scholar]
  68. Mod HK, Luoto M. Arctic shrubification mediates the impacts of warming climate on changes to tundra vegetation. Environmental Research Letters. 2016;11 doi: 10.1088/1748-9326/11/12/124028. 124028. [DOI] [Google Scholar]
  69. Montserrat P, Fillat F. The system of grassland management in Spain. Managed Grasslands Regional Studies. 1990;17:37–70. [Google Scholar]
  70. Morrison L, Estrada A, Early R. Species traits suggest European mammals facing the greatest climate change are also least able to colonize new locations. Diversity and Distributions. 2018;24:1321–1332. doi: 10.1111/ddi.12769. [DOI] [Google Scholar]
  71. Mottet A, Ladet S, Coqué N, Gibon A. Agricultural land-use change and its drivers in mountain landscapes: A case study in the Pyrenees. Agriculture, Ecosystems & Environment. 2006;114:296–310. doi: 10.1016/j.agee.2005.11.017. [DOI] [Google Scholar]
  72. Naito AT, Cairns DM. Patterns and processes of global shrub expansion. Progress in Physical Geography. 2011;35:423–442. doi: 10.1177/0309133311403538. [DOI] [Google Scholar]
  73. Nussey DH, Clutton-Brock TH, Albon SD, Pemberton J, Kruuk LE. Constraints on plastic responses to climate variation in red deer. Biology Letters. 2005;1:457–460. doi: 10.1098/rsbl.2005.0352. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Ogle DH. FSA: Fisheries stock analysis. R package version 0.8.17. 2017 [Google Scholar]
  75. Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, et al. Wagner H. Vegan: Community Ecology Package. R Package 2.4-5. 2017 [Google Scholar]
  76. Olofsson J, Oksanen L, Callaghan T, Hulme PE, Oksanen T, Suominen O. Herbivores inhibit climate-driven shrub expansion on the tundra. Global Change Biology. 2009;15:2681–2693. doi: 10.1111/j.1365-2486.2009.01935.x. [DOI] [Google Scholar]
  77. Olsen FW, Hansen RM. Food relations of wild free-roaming horses to livestock and big game, Red Desert, Wyoming. Journal of Range Management. 1977;30:17–20. doi: 10.2307/3897326. [DOI] [Google Scholar]
  78. Olsson EGA, Austrheim G, Grenne SN. Landscape change patterns in mountains, land use and environmental diversity, Mid-Norway 1960-1993. Landscape Ecology. 2000;15:155–170. doi: 10.1023/A:1008173628016. [DOI] [Google Scholar]
  79. Parmesan C, Yohe G. A globally coherent fingerprint of climate change impacts across natural systems. Nature. 2003;421:37–42. doi: 10.1038/nature01286. [DOI] [PubMed] [Google Scholar]
  80. Peñuelas J, Ogaya R, Boada M, Jump A. Migration, invasion and decline: Changes in recruitment and forest structure in a warming-linked shift of European beech forest in Catalonia (NE Spain) Ecography. 2007;30:829–837. doi: 10.1111/j.2007.0906-7590.05247.x. [DOI] [Google Scholar]
  81. Pereira HM, Leadley PW, Proenca V, Alkemade R, Scharlemann JPW, Fernandez-Manjarrés JF, et al. Walpole M. Scenarios for global biodiversity in the 21st century. Science. 2010;330:1496–1501. doi: 10.1126/science.1196624. [DOI] [PubMed] [Google Scholar]
  82. Poyatos R, Latron J, Llorens P. Land use and land cover change after agricultural abandonment. Mountain Research and Development. 2003;23:362–368. doi: 10.1659/0276-4741(2003)023[0362:LUALCC]2.0.CO;2. [DOI] [Google Scholar]
  83. Prévosto B, Kuiters L, Bernhardt-Römermann M, Dölle M, Schmidt W, Hoffmann M, et al. Brandl R. Impacts of land abandonment on vegetation: Successional pathways in European habitats. Folia Geobotanica. 2011;46:303–325. doi: 10.1007/s12224-010-9096-z. [DOI] [Google Scholar]
  84. R Core Team. A language and environment for statistical computing. 2018 [Google Scholar]
  85. Root T, Price J, Hall K, Schneider S, Rosenzweig C, Pounds JA. Fingerprints of global warming on wild animals and plants. Nature. 2003;421:57–60. doi: 10.1038/nature01333. [DOI] [PubMed] [Google Scholar]
  86. Rotenberry JT, Wiens JA. Habitat structure, patchiness, and avian communities in North American steppe vegetation: A multivariate analysis. Ecology. 1980;61:1228–1250. doi: 10.2307/1936840. [DOI] [Google Scholar]
  87. Roura-Pascual N, Pons P, Etienne M, Lambert B. Transformation of a rural landscape in the Eastern Pyrenees between 1953 and 2000. Mountain Research and Development. 2005;25:252–261. doi: 10.1659/0276-4741(2005)025[0252:TOARLI]2.0.CO;2. [DOI] [Google Scholar]
  88. Salter RE, Hudson RJ. Feeding ecology of feral horses in Western Alberta. Journal of Range Management. 1979;32:221–225. doi: 10.2307/3897127. [DOI] [Google Scholar]
  89. Sanz-Elorza M, Dana ED, González A, Sobrino E. Changes in the high-mountain vegetation of the central Iberian Peninsula as a probable sign of global warming. Annals of Botany. 2003;92:273–280. doi: 10.1093/aob/mcg130. [DOI] [PMC free article] [PubMed] [Google Scholar]
  90. Scasta JD, Beck JL, Angwin CJ. Meta-analysis of diet composition and potential conflict of wild horses with livestock and wild ungulates on Western Rangelands of North America. Rangeland Ecology & Management. 2016;69:310–318. doi: 10.1016/j.rama.2016.01.001. [DOI] [Google Scholar]
  91. Scherf B, editor. World watch list for domestic animal diversity. Rome, Italy: Food and Agriculture Organization (FAO); 2000. [Google Scholar]
  92. Schmitz OJ. Herbivory from individuals to ecosystems. Annual Review of Ecology, Evolution, and Systematics. 2008;39:133–152. doi: 10.1146/annurev.ecolsys.39.110707.173418. [DOI] [Google Scholar]
  93. Schulze KA, Rosenthal G, Peringer A. Intermediate foraging large herbivores maintain semi-open habitats in wilderness landscape simulations. Ecological Modelling. 2018;379:10–21. doi: 10.1016/j.ecolmodel.2018.04.002. [DOI] [Google Scholar]
  94. Scornavacca D, Lovari S, Cotza A, Bernardini S, Brunetti C, Pietrocini V, Ferretti F. Pasture quality affects juvenile survival through reduced maternal care in a mountain-dwelling ungulate. Ethology. 2016;122:807–817. doi: 10.1111/eth.12530. [DOI] [Google Scholar]
  95. Sherman DM. Tending animals in the global village. Troy D, editor. Journal of Veterinary Medical Education. 2005;32:156–162. doi: 10.3138/jvme.32.2.156. [DOI] [PubMed] [Google Scholar]
  96. Smit IPJ, Prins HHT. Predicting the effects of woody encroachment on mammal communities, grazing biomass and fire frequency in African Savannas. PLoS ONE. 2015;10:e0137857. doi: 10.1371/journal.pone.0137857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  97. Smith EP. Niche breadth, resource availability, and inference. Ecology. 1982;63:1675–1681. doi: 10.2307/1940109. [DOI] [Google Scholar]
  98. Somero GN. The physiology of climate change: How potentials for acclimatization and genetic adaptation will determine “winners” and “losers”. Journal of Experimental Biology. 2010;213:912–920. doi: 10.1242/jeb.037473. [DOI] [PubMed] [Google Scholar]
  99. Stanton RA, Boone WW, Soto-Shoender J, Fletcher RJ, Blaum N, McCleery RA. Shrub encroachment and vertebrate diversity: A global meta-analysis. Global Ecology and Biogeography. 2018;27:368–379. doi: 10.1111/geb.12675. [DOI] [Google Scholar]
  100. Steffen W, Rockström J, Richardson K, Lenton TM, Folke C, Liverman D, et al. Schellnhuber HJ. Trajectories of the Earth system in the anthropocene. Proceedings of the National Academy of Sciences. 2018;115:8252–8259. doi: 10.1073/pnas.1810141115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  101. Steffen W, Sanderson RA, Tyson PD, Jäger J, Matson PA, Moore B III, et al.Wasson RJ, editors. Global Change and the Earth System: A Planet Under Pressure. Berlin/Heidelberg: Springer-Verlag; 2005. [Google Scholar]
  102. Steinbauer MJ, Grytnes J-A, Jurasinski G, Kulonen A, Lenoir J, Pauli H, et al. Wipf S. Accelerated increase in plant species richness on mountain summits is linked to warming. Nature. 2018;556:231–234. doi: 10.1038/s41586-018-0005-6. [DOI] [PubMed] [Google Scholar]
  103. Stewart DRM. Analysis of plant epidermis in faeces: A technique for studying the food preferences of grazing herbivores. Journal of Applied Ecology. 1967;4:83–111. doi: 10.2307/2401411. [DOI] [Google Scholar]
  104. Sturaro E, Cocca G, Fuser S, Ramanzin M. Relationships between livestock production systems and landscape changes in the Belluno province. Italian Journal of Animal Science. 2005;4:184–186. doi: 10.4081/ijas.2005.2s.184. [DOI] [Google Scholar]
  105. Taberlet P, Valentini A, Rezaei HR, Naderi S, Pompanon F, Negrini R, Ajmone-Marsan P. Are cattle, sheep, and goats endangered species? Molecular Ecology. 2008;17:275–284. doi: 10.1111/j.1365-294X.2007.03475.x. [DOI] [PubMed] [Google Scholar]
  106. Tape K, Sturm M, Racine C. The evidence for shrub expansion in Northern Alaska and the Pan-Arctic. Global Change Biology. 2006;12:686–702. doi: 10.1111/j.1365-2486.2006.01128.x. [DOI] [Google Scholar]
  107. Tasser E, Tappeiner U. Impact of land use changes on mountain vegetation. Applied Vegetation Science. 2002;5:173–184. doi: 10.1111/j.1654-109X.2002.tb00547.x. [DOI] [Google Scholar]
  108. Tasser E, Walde J, Tappeiner U, Teutsch A, Noggler W. Land-use changes and natural reforestation in the Eastern Central Alps. Agriculture, Ecosystems and Environment. 2007;118:115–129. doi: 10.1016/j.agee.2006.05.004. [DOI] [Google Scholar]
  109. Thuiller W, Lavorel S, Araújo MB. Niche properties and geographical extent as predictors of species sensitivity to climate change. Global Ecology and Biogeography. 2005;14:347–357. doi: 10.1111/j.1466-822X.2005.00162.x. [DOI] [Google Scholar]
  110. Vacquié LA, Houet T, Sheeren D, de Munnik N, Roussel V, Waddle J. Adapting grazing practices to limit the reforestation of mountainous summer pastures: A process-based approach. Environmental Modelling and Software. 2016;84:395–411. doi: 10.1016/j.envsoft.2016.05.006. [DOI] [Google Scholar]
  111. Verburg PH, van Berkel DB, van Doorn AM, van Eupen M, van den Heiligenberg HARM. Trajectories of land use change in Europe: A model-based exploration of rural futures. Landscape Ecology. 2010;25:217–232. doi: 10.1007/s10980-009-9347-7. [DOI] [Google Scholar]
  112. Verrier E, Tixier-Boichard M, Bernigaud R, Naves M. Conservation and value of local livestock breeds: Usefulness of niche products and/or adaptation to specific environments. Animal Genetic Resources Information. 2005;36:21–31. doi: 10.1017/S1014233900005538. [DOI] [Google Scholar]
  113. Vigo J. L’Alta muntanya catalana : Flora i vegetació. 2nd ed. Barcelona: Editorial Institut d’Estudis Catalans; 2008. p. 443. [Google Scholar]
  114. Villamuelas M, Fernández N, Albanell E, Gálvez-Cerón A, Bartolomé J, Mentaberre G, et al. Serrano E. The Enhanced Vegetation Index (EVI) as a proxy for diet quality and composition in a mountain ungulate. Ecological Indicators. 2016;61:658–666. doi: 10.1016/j.ecolind.2015.10.017. [DOI] [Google Scholar]
  115. Vitousek PM, Mooney HA, Lubchenco J, Melillo JM. Human domination of earth’s ecosystems. Science. 1997;277:494–499. doi: 10.1126/science.277.5325.494. [DOI] [Google Scholar]
  116. Wallentin G, Tappeiner U, Strobl J, Tasser E. Understanding alpine tree line dynamics: An individual-based model. Ecological Modelling. 2008;218:235–246. doi: 10.1016/j.ecolmodel.2008.07.005. [DOI] [Google Scholar]
  117. Wilson JB, Peet RK, Dengler J, Pärtel M. Plant species richness: The world records. Journal of Vegetation Science. 2012;23:796–802. doi: 10.1111/j.1654-1103.2012.01400.x. [DOI] [Google Scholar]
  118. Yockney IJ, Hickling GJ. Distribution and diet of chamois (Rupicapra rupicapra) in Westland forests, South Island, New Zealand. New Zealand Journal of Ecology. 2000;24:31–38. [Google Scholar]

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