Polar Biology (2019) 42:1561–1570 https://doi.org/10.1007/s00300-019-02543-y

ORIGINAL PAPER

Combined efects of simulated browsing, warming and nutrient addition on forage availability for migratory caribou in Nunavik, Canada

Valérie Saucier1 · Emilie Champagne1,2 · Steeve D. Côté1 · Jean‑Pierre Tremblay1,2

Received: 23 July 2018 / Revised: 29 May 2019 / Accepted: 9 July 2019 / Published online: 30 July 2019 © Springer-Verlag GmbH Germany, part of Springer Nature 2019

Abstract At high population size, migratory caribou (Rangifer tarandus) are regulated by forage abundance in their summer range. Climate warming likely afects forage availability by increasing productivity and advancing phenology of vegetation. Our objective was to investigate the combined efects of browsing and climate warming on the availability of dwarf birch (Betula glandulosa). We simulated direct (warming, with open-top chambers) and indirect (increased nutrient cycling) efects of climate warming in interaction with simulated browsing (leaf stripping) from 2009 to 2013 in Nunavik, Canada. We meas- ured the efect of treatments on dwarf birch biomass and phenology. Moderate and heavy browsing reduced the estimated biomass of birch leaves by 14% and 34%, respectively. Fertilization did not increase the biomass of birch leaves, but increased the biomass of another forage, Poaceae. The warming treatment advanced the opening of birch leaves by 4 days (95% CI: [3, 6]) in 2011 and 7 [5, 8] days in 2013, the two years colder than average. The absence of signifcant phenological shifts in warmed plots during warmer springs suggests that established dwarf birches may have reached a threshold in a limiting resource, likely soil moisture, under which they cannot respond to further warming. Our results demonstrate that browsing can reduce forage biomass, but the variability in caribou populations could provide windows of opportunity for shrub growth.

Keywords Betula glandulosa · Climate change · Herbaceous arctic tundra · Phenology · Rangifer tarandus

Introduction forage to restore their body condition (Klein 1990) and pro- duce milk (Taillon et al. 2013) that calves rely on for their At high population size, migratory caribou (Rangifer taran- growth (Cebrian et al. 2008; Post et al. 2008). Erect decidu- dus Linnaeus, 1758 subsp caribou) are likely regulated by ous shrubs, such as willows (Salix spp.) and dwarf birches the availability of summer forage (Messier et al. 1988). For- (Betula glandulosa Michx. and B. nana L.), can be a major age availability in early summer is crucial for the recon- source of protein for caribou in summer (Crête et al. 1990; stitution of body mass and growth of caribou (Gunn and Klein 1990). They also are the dominant species involved in Skogland 1997). Females rely on the protein content of the densifcation of erected shrubs observed in Arctic and sub-Arctic ecosystems (Myers-Smith et al. 2011; Elmendorf et al. 2012; Ropars and Boudreau 2012). Understanding how Electronic supplementary material The online version of this forage availability will be modifed by the response of shrubs article (https​://doi.org/10.1007/s0030​0-019-02543​-y) contains to climate changes appears fundamental to our understand- supplementary material, which is available to authorized users. ing of migratory caribou population ecology. * Jean‑Pierre Tremblay Shrub densifcation is driven by warming temperatures Jean‑[email protected] and accelerated by feedback loops (Myers-Smith et al.

1 2011). For example, shrub densifcation can increase snow Département de Biologie, Centre D’Études Nordiques cover and thus soil temperature, consequently increasing and Caribou Ungava, Université Laval, 1045 ave de la Médecine, Pavillon Vachon, Québec, QC G1V 06, Canada microbial activity and nutrient availability further promot- ing shrub growth (Sturm et al. 2005). This positive efect of 2 Centre D’Études de La Forêt, Université Laval, 2405 Rue de la Terrasse, Pavillon Abitibi‑Price, Québec, QC G1V 06, climate warming on forage biomass could be counteracted Canada by the browsing of Arctic herbivores (Olofsson et al. 2009;

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Ravolainen et al. 2011). For example, biomass and height predicted a positive efect of warming with open top cham- of Betula nana were higher in reindeer (Rangifer tarandus bers and nitrogen fertilization on the biomass of dwarf birch subsp platyrhynchus) and small mammals exclosures (Olof- leaves only under low or no simulated browsing pressures. sson et al. 2009), and cumulative browsing over multiple Because caribou feed extensively on Poaceae before the years reduced radial growth in Betula glandulosa (Morris- opening of shrub leaves (Crête et al. 1990), we also meas- sette-Boileau et al. 2018a). ured the biomass of Poaceae expecting positive responses Climate warming is also known to lengthen the growing independent of browsing pressure in species with a basal season by advancing spring (Linderholm 2006) and delaying meristem. Finally, we expected earlier bud burst and leaf fall (Jeong et al. 2011). Populations of migratory caribou opening of dwarf birch in warmed plots independent of other are closely related to plant phenology, mainly because calf factors. recruitment depends on protein-rich forage (Post and Klein 1999). From fall to the following spring, caribou forage mainly on lichens with a low protein content (Klein 1990), Materials and methods leading to a negative protein balance for 7 months a year (Gerhart et al. 1996). Thus, an advance in plants phenol- Study area ogy could lead to a mismatch between the availability of protein-rich forage and protein requirements in spring and Our study site was located near Deception Bay (N62.08′41″, early summer (Stenseth 2002; Post et al. 2008; Gauthier W74.41′52″; Québec, Canada; Fig. 1), within the summer et al. 2013). A mismatch has been shown to decrease the range of the Rivière-aux-Feuilles migratory caribou herd recruitment of calves in caribou (Post et al. 2008). (Taillon et al. 2012). The Rivière-aux-Feuilles herd reached Our objective was to investigate the combined efects of 1,193,000 ± 47.5% individuals in 2001 (Couturier et al. browsing, warming and fertilization on the availability of 2004) but was estimated at 430,000 ± 23% individuals at Betula glandulosa (hereafter dwarf birch) in summer for the time of this study (2011; Québec Government aerial caribou. Dwarf birch can be a main constituent of the diet survey, unpubl. data). The herd is still declining and was of caribou (Crête et al. 1990) and its protein content when estimated at 199,000 ± 8% in 2016 (Québec Government leaves open is higher than in many other plants (Klein 1990), aerial survey, unpubl. data). The bedrock geology consists although it is high in triterpenes and could be less digest- of foliated granite and granitic gneiss (Agriculture and Agri- ible than other resources (Bryant et al. 2014). We hypoth- Food Canada 2013) and the surfcial material is composed esized that browsing by caribou can counteract the expected of till veneer (Fulton 1995) and is underlain by continuous positive efects of climate warming on forage availability, permafrost. The vegetation at the study site is typical of the through longer growing seasons and more fertile soils, as Arctic herbaceous tundra bioclimatic region (Ministère des it removes photosynthetic tissues on the shrubs. In addi- Ressources Naturelles et de la Faune 2003) is essentially tion, warming and/or fertilization could advance the tim- composed of bryophytes, Poaceae (mainly Calamagrostis ing of dwarf birch leaves development in early summer. We lapponica (Wahlenb.) Hartm., Hierochloë alpina alpina

Fig. 1 Location of the study area at Deception Bay, Nunavik, Canada (Base map credits: Esri, HERE, Garmin, OpenStreetMap contributors, and the GIS user community)

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(Sw. ex Willd.) Roem. & Schult, and Eriophorum angus- 2014). We applied the browsing treatment to all distal twigs tifolium subsp. angustifolium Honck.), evergreen shrubs in a 1 × 1 m subplot within 4 × 4 m plots when ca. 75% of (mainly Vaccinium vitis-idaea L. and Vaccinium uligino- birch leaves had opened, which approximately corresponds sum L.) and deciduous shrubs (mainly B. glandulosa and to the moment when caribou were observed stripping ramets Salix spp.; Walker et al. 2005). Gauthier et al. (1989) found (Online resource 1; Bergerud et al. 2008). B. glandulosa leaves in 25% of rumen from the George- River herd caribou sampled in June, while Crête et al. (1990) Forage biomass reported that shrub leaves and twigs constituted respectively 54% (SE = 2) and 12% (SE = 1) of rumen content in July for We estimated the biomass of dwarf birch leaves in the sub- the Rivière-aux-Feuilles herd. In spring, mean temperatures plots in early August of each year using the point intercept are between − 2 and − 4 °C and mean annual precipitation method with 25 systematic points within a 75 × 75 cm frame ranges from 100 to 150 mm for the 1981–2010 period (April on the 1 × 1 m browsing subplot (Jonasson 1988; Bråthen to June; Environment Canada 2014). and Hagberg 2004). To validate the method, we applied the point intercept protocol to 32 plots outside of the treated Experimental design blocks and destructively harvested birch leaves within those plots. We dried these samples and correlated the number In 2009, we implemented a simulation experiment to manip- of intercepts on dwarf birch leaves with their dry biomass. ulate temperature (warming) and soil nutrient (fertilization) The number of intercepts on birch leaves explained a large in interaction with caribou browsing pressure on dwarf proportion of the variance in leaf biomass (R2 = 0.80) con- birch. The split-plot experimental design included two levels frming that the number of intercepts is an acceptable proxy of fertilization in 4 × 24 m main plots where we randomly of the biomass of birch leaves (Online resource 2). Because allocated two levels of warming crossed with three levels of caribou feed extensively on Poaceae before the opening of simulated summer browsing in 4 × 4 m plots (Morrissette- shrub leaves (Crête et al. 1990), we also measured the bio- Boileau et al. 2018a). We replicated the factorial combi- mass of Poaceae available in the browsing subplots, using nation of the three treatments (fertilization, warming and the same method in the 48 plots. Calamagrostis lapponica, browsing) in fve blocks where caribou were excluded by Hierochloë alpina alpina and Poa arctica R. Br. subsp. arc- 12 × 26 × 1.5 m wire fences for a total of 60 plots. We cut tica where the dominant Poacea species in our plots. The trenches between plots to isolate birch clones. All blocks number of intercepts of Poaceae predicted a large proportion were located on a south-west facing hill dominated by dwarf of the variance in the biomass of Poaceae (R2 = 0.78; Online birch (slope between 1 and 11%; see Champagne et al. 2012 resource 2). for details on orientation of the block and snow depth accu- mulation). We fertilized plots located downslope, to limit Phenological responses of dwarf birch runof toward unfertilized plots, with 10 g nitrogen m­ −2 in 2009 to 2011 in the form of granular urea at the begin- We tracked the phenological responses of dwarf birch in ning of bud burst in early June (Online resource 1) follow- each subplot every 3 days from June to August 2010 to 2013. ing the experiment of Toolik Lake, Alaska (Chapin et al. We used two discrete stages of dwarf birch phenological 1995; Bret-Harte et al. 2001). We reduced the fertilization to development: bud burst and opening of 75% of leaves. The 1 gnitrogen ­m−2 in 2012–2013 to represent a more realistic onset of a stage corresponded to the frst observation of a N addition in the soil induced by climate warming (Zamin plant at that stage in each plot (Molau 1997). We used bud and Grogan 2012). We used hexagonal open top chambers burst as an indication of the beginning of the plant growing (OTCs) to simulate warming from early June to mid-August season. The opening of 75% of leaves was associated with following the protocol of the International Tundra Experi- the peak of consumption by caribou (Bergerud et al. 2008). ment (Henry and Molau 1997; Marion et al. 1997). We To understand phenological responses in the context of simulated caribou browsing by stripping available shoots climatic conditions and local climate warming, we calcu- (distal twig ≥ 5 cm and ≤ 12 cm; Champagne et al. 2012) of lated the accumulation of degrees over 0 °C during May and their leaves (Online resource 1). We chose unequal levels of June (thawing degree-days). We used thawing degree-days summer caribou browsing (0%, 25% and 75% of available instead of growing degree-days above 5 °C since the phenol- shoots) because we suspected a non-linear response at the ogy of Arctic plants shows good correlations with the former extreme of the browsing treatment on the dependent vari- (Lévesque et al. 1997; Pop et al. 2000). We used temperature ables (Leik 1997). Removal of leaves on 75% of available estimates at 2 m in the air from the NCEP North American twigs likely corresponds to heavy browsing pressure encoun- Regional Reanalysis (NARR; Mesinger et al. 2006) pro- tered when caribou populations are high (Manseau et al. vided by the NOAA/OAR/ESRL PSD (Boulder, Colorado, 1996) or when the availability of birch is low (Plante et al. USA, available at https://www.esrl.noaa.gov/psd/​ ). We used

1 3 1564 Polar Biology (2019) 42:1561–1570 estimates from 2010 to 2013, every 3 h, from 8 pixels of we added the phenological stage as a repeated measure to 32 × 32 km centered on the study area; we removed one pixel model its multivariate covariance structure. For all analyses, located over the Hudson Strait. We also used the NARR we visually assessed homogeneity of variance and the nor- monthly estimates from 1979 to 2014 to evaluate spring mality of residuals. We applied square root transformations temperature trends (May to June) in the same pixels. The when required. When efects were the same between raw NCEP Reanalysis data are highly correlated to the spring and transformed data, we used raw data to conduct analyses month (May and June) temperatures measured at the closest (Conover 1999). We conducted mean comparisons with pol- weather station ( ± 60 km) in Salluit, between 2003 and 2014 ynomial contrasts whenever year was involved for biomass (Pearson R = 0.82 and 0.98, p = 0.003 and < 0.001, for May (CONTRAST statement; SAS Institute 2012) and used least and June, respectively; Centre for Nordic Studies 2010) and square means for all other comparisons (LSMEANS state- to daily temperature estimate from a local weather station ment; SAS Institute 2012). Data are presented as untrans- (HOBO U30-NRC Weather Station, Onset, Bourne, MA) formed model estimates ( x̄ [95% CI]). All statistical analyses that was in function from mid-June to August (Pearson were performed with SAS 9.3 (SAS Institute 2012) with R = 0.88, p < 0.001 for 2010–2013). α = 0.05.

Statistical analyses Results We used general linear mixed models (MIXED procedure; SAS Institute 2012) to examine the efects of fertilization, Forage biomass warming, browsing, years and all three-way interactions between these variables included as fxed efects on the Fertilization did not increase the estimated biomass of birch estimated biomass (number of intercepts) of birch leaves leaves, however, the estimated biomass of Poaceae signif- and Poaceae. We computed block as a random factor and cantly increased with time in fertilized and unfertilized year as a repeated measure in mixed models (see Table 1). plots, although at a lower rate in the latter (Table 1; Fig. 2). When analyzing the phenology (number of days since 31 Warmed plots had 13% less biomass of dwarf birch leaves May) of bud burst and opening of 75% of dwarf birch leaves, than plots at ambient temperature (35 leaf intercepts [95%

Table 1 Analyses of variance (ANOVAs) testing the efects of fer- block (n = 5) as a random factor and year (n = 5) as a repeated meas- tilization, warming and browsing pressure on the estimated biomass ure. When analyzing phenology (number of days since 31 May) of (number of leaf intercepts) of Poaceae and the estimated biomass and bud burst and opening of 75% of dwarf birch leaves, we included the phenology of dwarf birch leaves (Betula glandulosa) in a simulation phenological stage as a repeated measure to model its multivariate experiment conducted for 5 years in the Arctic tundra at Deception covariance structure. Signifcant p values (α = 0.05) are indicated in Bay (Nunavik, Canada). We used general linear mixed models with bold.

Poaceae Dwarf birch Estimated biomass Estimated biomass Phenology df F P df F P df F P

Fertilization (F) 1,4 53.8 0.002 1,4 4.6 0.10 2,8 1.3 0.33 Warming (W) 1,40 2.9 0.10 1,40 4.8 0.03 2,8 29.7 0.0003 F × W 1,40 0.8 0.37 1,40 0.2 0.63 2,8 0.3 0.77 Browsing (B) 2,40 1.2 0.31 2,40 12.6 < 0.0001 4,16 1.0 0.42 F × B 2,40 2.7 0.08 2,40 1.1 0.33 4,16 1.6 0.23 W × B 2,40 0.3 0.75 2,40 0.3 0.76 4,16 0.5 0.73 F × W × B 2,40 0.8 0.48 2,40 0.2 0.82 4,16 1.1 0.37 Year (Y) 4,190 47.9 < 0.0001 4,191 3.0 0.02 6,24 588.5 < 0.0001 F × Y 4,190 13.7 < 0.0001 4,191 2.0 0.10 6,24 1.1 0.37 W × Y 4,190 1.2 0.33 4,191 1.5 0.22 6,24 15.8 < 0.0001 F × W × Y 4,190 1.4 0.22 4,191 0.9 0.44 6,24 1.7 0.16 B × Y 8,190 0.6 0.82 8,191 1.5 0.17 12,48 0.9 0.58 F × B × Y 8,190 0.7 0.70 8,191 1.5 0.16 12,48 1.1 0.38 W × B × Y 8,190 1.1 0.34 8,191 0.6 0.76 12,48 1.1 0.37 F × W × B × Y 8,190 0.7 0.67 8,191 0.4 0.92 12,47 0.7 0.78

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Phenological responses

Simulated warming was the only treatment that advanced the phenological development of dwarf birch leaves in 2011 and in 2013 (Table 1; Fig. 3). In 2011, bud burst was advanced by 2 [2, 3] days in warmed plots relative to control plots (t28 = 6.61, p < 0.0001; Fig. 3). The efect of the warming treatment on the timing of bud burst was irrelevant in 2010 and 2012 because the reinstallation of the OTCs coincided with bud burst (Fig. 3 and Online resource 1). The opening of 75% of leaves was advanced by 4 [3, 6] days in 2011 (t28 = 5.28, p < 0.0001) and 7 [5, 8] days in 2013 (t28 = 8.79, p < 0.0001; Fig. 3). We did not detect any efect of warming Fig. 2 Changes in the estimated biomass of Poaceae (number of leaf in years with the fastest accumulation of thawing degree- intercepts) from 2 levels of fertilization through 5 years of experi- days in early June (2010 and 2012; Fig. 3). The NARR mental treatment in the Arctic tundra at Deception Bay (Nunavik, estimates showed that those years had the highest mean Canada). The curves represent polynomial contrasts following a linear mixed model with block (n = 5) as a random factor and year temperatures in May–June, higher than the average for the (n = 5) as a repeated measure 1979–2014 period (Fig. 4). Inversely, the mean temperatures in May–June for 2011 and 2013 were below the 1979–2014 average (Fig. 4). CI: 31, 38] versus 40 [36, 44]; Table 1); the warming treat- ment did not increase the biomass of Poaceae (30 [23, 37] versus 36 [29, 44]; Table 1). Independently of all other treat- Discussion ments, heavy browsing reduced the biomass of birch leaves by 34% compared to unbrowsed plots (30 leaf intercepts Using simulated caribou browsing on dwarf birch for 5 years [25, 34] and 44 [40, 48], respectively; t40 = 4.97, p < 0.0001, in plots with manipulated levels of temperature and fertiliza- Table 1) and by 20% compared to moderately browsed plots tion, we observed a much larger negative efect of browsing (38 leaf intercepts [34, 43]; t40 = 3.04, p = 0.004). Moderate on the biomass of B. glandulosa than the positive efects browsing also tended to reduce the biomass of birch by 14% of fertilization or the neutral efect of warming. This pro- compared to unbrowsed plots (t40 = 1.93, p = 0.06, Table 1). vides support for the hypothesis that large herbivores have

Fig. 3 Thawing degree days accumulation (TDD; sum of degrees (α = 0.05) following a linear mixed model with block (n = 5) as a ran- above 0 °C) at Deception Bay (Nunavik, Canada) during the pheno- dom factor and year (n = 4) as a repeated measure. Standard error is logical development of dwarf birch (Betula glandulosa) in a simu- 0.4 day for bud burst and 0.6 day for leaves opening. The efect of lation experiment. Phenological stages are presented for warmed the warming treatment on the timing of budburst could not be evalu- plots using open-top chambers and plots under ambient temperature. ated in 2010, 2012, and 2013 because the application of the treatment Signifcant diferences due to the warming treatment are indicated (black bar on the x-axis) coincided with budburst by Asterisk, based on a posteriori least square mean diferences

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Fig. 4 Mean air temperature at 2 m estimated by the NCEP North American regional reanalysis (NARR) from May to June. Each point is the average from the two months over 8 pixels of 32 × 32 km centered on the study area. The dotted line is the average for the 1979–2014 period. The grey region covers the study period (2009, 2013)

the potential to outmatch the efect of climate change in 1996; Olofsson et al. 2009). Although birches could com- low productivity herbaceous Arctic tundra. Although our pensate for moderate browsing (Champagne et al. 2012), study focused on dwarf birch, the simulation of increased chronic browsing sustained over 5 years can reduce birch soil nutrients through fertilization benefted Poaceae which biomass. In a destructive sampling of birch stems from our increased in biomass with the repetition of the treatment experiment, Morrissette-Boileau et al. (2018a) also showed over 5 years. In addition, simulated warming advanced the a cumulative negative impact of browsing on radial growth, timing of vegetative phenological stages of dwarf birch such although they could not detect any efect of browsing on as bud burst and opening of leaves in cold years. Tempera- total aboveground biomass. Under the actual warmer cli- tures have been increasing in Nunavik since 1970 (Fortier mate regime, Morrissette-Boileau (2018b) observed a high et al. 2011). In the warmest years of our experiment, addi- recruitment of small B. glandulosa ( < 100 ­cm2 in crown tional warming could not further advance opening of leaves. size) in our study area, but their size is still too small to detect any changes in shrub cover over time (Plante et al. Forage biomass 2014). The role of browsing on the availability of birch as a forage source in summer will depend on the capacity of The simulation of climate warming with open-top chambers caribou to limit birch growth and the development of their (OTCs) led to a 13% reduction in the estimated biomass of vertical structure (Morrissette-Boileau 2018b). dwarf birch leaves in opposition with the implicit predic- The fertilization treatment did not increase the biomass tion that warming should increase the primary production of of birch leaves, possibly because it unbalanced the soil dwarf shrubs. OTCs are expected to increase temperature by nitrogen and phosphorus stoichiometry. Tundra ecosys- 1.2 to 1.8 °C, but they are also known to alter other ecologi- tems are also limited in phosphorus availability and addi- cal factors such as lower wind, thus reducing forced convec- tion of nitrogen without phosphorus can preclude biomass tive heat loss, slightly lower relative humidity because of response of birches (Elser et al. 2007; Zamin and Grogan increase temperature and lower soil moisture due to evapo- 2012) or reduce the efect of nitrogen over time (Street transpiration (Marion et al. 1997). The earlier onset of bud et al. 2015). Alternatively, Zamin and Grogan (2012) have burst and opening of leaves in OTCs in colder years of the suggested that a threshold in nitrogen availability must be experiment suggests that passive warming did occur, but that reached for B. glandulosa to respond to the fertilization; other factors were involved. Considering the dry conditions in their study, no apical stem growth was observed after of our study area, soil moisture could have become limit- 6 years of low-level nitrogen addition. Street et al (2015) ing during warm years, reducing the growth of dwarf birch also reported a negative efect of fertilization, with nitrogen (Dunne et al. 2003). only or in combination with phosphorus, on the survival of In these conditions, the top-down efect of browsing was dwarf shrubs in tundra heath following ice-encasement of the dominant factor afecting the biomass of dwarf birch vegetation in winter due to delayed hardening. Poaceae are compared to the bottom-up efects of warming and fertiliza- known to beneft from fertilization (Aerts et al. 2006) and tion. Previous studies indicated that browsing by herbivores responded accordingly in our study area. A shift in domi- could limit the expansion of dwarf shrubs (Manseau et al. nance from dwarf shrubs to Poaceae would likely change the

1 3 Polar Biology (2019) 42:1561–1570 1567 nutritional value of forage available to caribou (Klein et al. a stronger driver of fowering phenology than spring tem- 2007). Although Poaceae are commonly used as forage by perature in four species from the high Arctic tracked over caribou, especially in spring, their protein content is lower 21 years (Bjorkman et al. 2015). than in dwarf shrub leaves in early summer, when caribou Changes in plant phenology infuence the nutritional have their highest nutrient requirements (Klein 1990). Yet, quality of forage, as N content decreases while fber content an increase in Poaceae could likely be a transient succes- increases over the growing season (Mårell et al. 2006; Doi- sional stage if shrubs start to respond to improve growing ron et al. 2014). Zamin et al. (2017) observed a decline in conditions and eventually shade the ground layer (Chapin leaf nitrogen concentrations in warmed plots in early sum- et al. 1995). Svalbard reindeer have been reported to select mer, a critical period for caribou lactation. Post et al. (2008) feeding patches based on quantity rather than quality (Van reported that the variability in the timing of calving date der Wal et al. 2000), suggesting that forage quality could be of caribou is usually more constrained than the phenology equally or less important than forage quantity (Mårell et al. of plants. Such conditions can lead to a trophic mismatch 2006). Nevertheless, changes in species composition due between the needs of caribou in a key period of their life to climate warming could infuence the nutritional ecology cycle and the availability of protein-rich birch leaves, and of caribou in a long-term scale, especially during crucial eventually a reduction in calf recruitment (Post and Forch- periods in their life cycle. hammer 2008). Moreover, change in the temporal dynamics of nitrogen, fber and secondary metabolites in plants could Phenological responses of dwarf birch still lead to mismatch between the availability of digestible proteins in plants and nutritional needs of animals (Doiron In ecosystems with a short growing season and high inter- et al. 2014). annual variability such as the tundra, plants should be able to respond quickly to change in environmental cues (Pau et al. 2011). However, limiting resources constraining the Conclusion possible advance of phenological stages such as leaf bud burst or leaf opening for plants growing under harsh Arc- Heavy browsing was the strongest driver of birch biomass in tic conditions could reduce the variability in birch phenol- our experimental study. Browsing pressure at the landscape ogy despite the increasing variability in temperature due scale is dependent on the abundance and spatial distribu- to climate change (IPCC 2014). The absence of signifcant tion of consumers and resources, thus potentially provid- phenological shifts in warmed plots during warmer springs ing birch with windows of opportunities to recover from (Fig. 3) suggests that dwarf birch may have reached a thresh- browsing when caribou populations are declining as they old in a limiting resource, likely soil moisture, under which are now. Inversely, directional climate warming could even- they cannot respond to further warming under the condi- tually stimulate the growth of small B. glandulosa recruits tions found in our study area (transient maxima hypothesis; if their abundance allows them to overcome the top-down Seasted and Knapp 1993). The largest shift in the phenol- control from browsing. Predicted warming may not fur- ogy of leaf opening in warmed plots (one week) occurred in ther advance the vegetative stages of established shrubs 2013, the fourth coldest spring estimated in our study area if specifc resources continue to limit growth unless new for the 1979–2014 period (Figs. 3 and 4). Moreover, birch recruits do not experience these limits under relaxed grow- leaves opened earlier in springs with temperature warmer ing conditions. than the 1979–2014 average and faster accumulation of thawing degree-days (2010 and 2012; Figs. 3 and 4). An Acknowledgments V. Saucier received scholarships from Caribou earlier meta-analysis of simulated warming experiments in Ungava, EnviroNord, Association of Canadian Universities for North- Arctic and sub-Arctic sites (Arft et al. 1999) revealed tem- ern Studies and the Beverly and Qamarniqjuak management board. poral variability in the leaf bud burst of deciduous shrubs. This project is part of the Caribou Ungava research program (https​ ://www.carib​ou-ungav​a.ulava​l.ca/en/accue​il/) funded by Natural Sci- Krab et al. (2018) experimentally demonstrated that warmer ences and Engineering Research Council (NSERC Grant no. CRDPJ spring temperature advanced green-up of dwarf shrubs com- 369122-08) of Canada, Ministère des Forêts, de la Faune et des Parcs munities compared to control plots at ambient temperature, du Québec, ArcticNet, Fonds de recherche du Québec nature et tech- only under conditions corresponding to average snowmelt nologies, Hydro Québec, Xstrata Nickel (now Glencore), Fédération des pourvoiries du Québec inc., Fédération québécoise des chasseurs et date. Indeed, temperature or accumulated heat are not the pêcheurs, First Air, Makivik Corporation, CircumArctic Rangifer Mon- only determinants of plant phenology, as shown by the late itoring and Assessment (CARMA), International Polar Year, Canada leaves opening in spring 2011, despite a heat accumulation Foundation for Innovation, Institute for Environmental Monitoring and curve similar to 2010 (Fig. 3). For example, snow cover Research, Fondation de la Faune du Québec, Ouranos, and the Cana- dian Wildlife Federation. We are particularly indebted to Glencore— and snowmelt were key determinants of bud burst in Betula Raglan Mine for their collaboration, logistic support and the continuous nana (Pop et al. 2000). The timing of snowmelt was also use of their infrastructures. The Quarqalik landholding corporation

1 3 1568 Polar Biology (2019) 42:1561–1570 of Salluit welcomed our team on their land. Thanks to Raglan Mine du Nord-du-Québec and Direction de la recherche sur la faune, employees, S. Lavoie, M. LeCorre, A.-A. Simard, A. Drolet, M. Bonin, Québec G. Daigle, M.-C. Martin, A. Brousseau, B. A. Campeau, and especially Crête M, Huot J, Gauthier L (1990) Food selection during early lacta- J. Boulanger-Pelletier, D. Côté-Vaillancourt and F. Dulude-de-Blouin tion by caribou calving on the tundra in Québec. Arctic 43:60–65. for their help with feld work. We are grateful to C. Hins and S. De https​://doi.org/10.14430​/arcti​c1592​ Bellefeuille for logistical help, to M. LeCorre for help with the NARR Doiron M, Gauthier G, Lévesque E (2014) Efects of experimen- data and to A. Drolet, M. Bonin, and S. Lavoie for reviewing an earlier tal warming on nitrogen concentration and biomass of forage version of this manuscript. plants for an arctic herbivore. J Ecol 102:508–517. https​://doi. org/10.1111/1365-2745.12213​ Compliance with ethical standards Dunne JA, Harte J, Taylor KJ (2003) Subalpine meadow fowering phenology responses to climate change: integrating experimental and gradient methods. Ecol Monogr 73:69–86 Conflict of interest The authors declare that they have no confict of Elmendorf SC et al (2012) Global assessment of experimental interest. climate warming on tundra vegetation: heterogeneity over space and time. Ecol Lett 15:164–175. https​://doi.org/10.111 1/j.1461-0248.2011.01716​.x Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, References Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE (2007) Global analysis of nitrogen and phosphorus limita- Aerts R, Cornelissen JHC, Dorrepaal E (2006) Plant performance in tion of primary producers in freshwater, marine and terrestrial a warmer world: general responses of plants from cold, northern ecosystems. Ecol Lett 10:1135–1142. https​://doi.org/10.111 biomes and the importance of winter and spring events. Plant Ecol 1/j.1461-0248.2007.01113​.x 182:65–77. https​://doi.org/10.1007/s1125​8-005-9031-1 Environment Canada (2014) Climatology of temperature and precipi- Agriculture and Agri-Food Canada (2013) National ecological frame- tation. Observation for June–July–August from the 1981–2010 work of Canada: Ecological Framework Attribute. https://sis.agr.​ period. https​://weath​er.gc.ca/saiso​ns/clim_e.html. Accessed 11 gc.ca/cansis/nsdb/ecost​ rat/1999r​ eport​ /data_table​ s.html​ . Accessed July 2014 4 Sept 2014 Fortier R, LeBlanc AM, Yu W (2011) Impacts of permafrost degrada- Arft AM et al (1999) Responses of tundra plants to experimental warm- tion on a road embankment at Umiujaq in Nunavik (Quebec), Can- ing: meta-analysis of the International Tundra Experiment. Ecol ada. Can Geotech J 48:720–740. https​://doi.org/10.1139/t10-101 Monog 69:491–511 Fulton RJ (1995) Surfcial materials of Canada, Geological Survey of Bergerud AT, Luttich SN, Camps L (2008) The return of Caribou to Canada, Map 1880A, 1:5,000,000. G.S.C, Ottawa Ungava. McGill-Queen’s University Press, Montreal Gauthier L, Nault R, Crête M (1989) Seasonal variation in the diet of Bjorkman AD, Elmendorf SC, Beamish AL, Vellend M, Henry GHR George River Caribou Herd, Québec. Nat Can 116:101–112 (in (2015) Contrasting efects of warming and increased snowfall on French) Arctic tundra plant phenology over the past two decades. Glob Gauthier G, Bety J, Cadieux MC, Legagneux P, Doiron M, Chevallier Change Biol 21:4651–4661. https​://doi.org/10.1111/gcb.13051​ C, Lai S, Tarroux A, Berteaux D (2013) Long-term monitoring Bråthen KA, Hagberg O (2004) More efcient estimation of plant bio- at multiple trophic levels suggests heterogeneity in responses to mass. J Veg Sci 15:653–660 climate change in the Canadian Arctic tundra. Phil Trans R Soc B Bret-Harte MS, Shaver GR, Zoerner JP, Johnstone JF, Wagner JL, 368:20120482. https​://doi.org/10.1098/rstb.2012.0482 Chavez AS, Gunkelman RF, Lippert SC, Laundre JA (2001) Gerhart KL, White RG, Cameron RD, Russell DE (1996) Body compo- Developmental plasticity allows Betula nana to dominate tundra sition and nutrient reserves of arctic caribou. Can J Zool 74:136– subjected to an altered environment. Ecology 82:18–32 146. https​://doi.org/10.1139/z96-018 Bryant JP, Joly K, Chapin SF, DeAngelis DL, Kielland K (2014) Can Gunn A, Skogland T (1997) Responses of caribou and reindeer to antibrowsing defense regulate the spread of woody vegetation in global warming. In: Oechel WC, Callaghan T, Gilmanov T, Holten Arctic tundra? Ecography 37:204–211. https​://doi.org/10.111 JI, Maxwell B, Molau U, Sveinbjörnsson B (eds) Global change 1/j.1600-0587.2013.00436​.x and arctic terrestrial ecosystems. Springer, New York, pp 189–200 Cebrian MR, Kielland K, Finstad G (2008) Forage quality and reindeer Henry GHR, Molau U (1997) Tundra plants and climate change: the productivity: multiplier efects amplifed by climate change. Arct International Tundra Experiment (ITEX). Glob Change Biol 3:1– Antarct Alp Res 40:48–54 9. https​://doi.org/10.1111/j.1365-2486.1997.gcb13​2.x Centre for Nordic Studies (2018) Climate station data from the Salluit IPCC (2014) Climate change 2014: synthesis report. In: Pachauri RK, Region in Nunavik, Quebec, Canada, v. 1.5 (1987–2017). Nordi- Meyer LA (eds) Contribution of working groups I. II and III to the cana D3. doi: 10.5885/45048SL-4708BCCDFA124359 ffth assessment report of the Intergovernmental Panel on Climate Champagne E, Tremblay JP, Côté SD (2012) Tolerance of an expand- Change, IPCC Geneva, p 151 ing subarctic shrub, Betula glandulosa, to simulated caribou Jeong SJ, Ho CH, Gim HJ, Brown ME (2011) Phenology shifts at start browsing. PLoS ONE 7:e51940. https​://doi.org/10.1371/journ​ vs. end of growing season in temperate vegetation over the North- al.pone.00519​40 ern Hemisphere for the period 1982–2008. Glob Change Biol Chapin FS, Shaver GR, Giblin AE, Nadelhoffer KJ, Laundre JA 17:2385–2399. https://doi.org/10.1111/j.1365-2486.2011.02397​ .x​ (1995) Responses of arctic tundra to experimental and observed Jonasson S (1988) Evaluation of the point intercept method for the changes in climate. Ecology 76:694–711. https://doi.org/10.111​ estimation of plant biomass. Oikos 52:101–106. https​://doi. 1/j.1365-2486.2005.00926​.x org/10.2307/35659​88 Conover WJ (1999) Practical nonparametric statistics, 3rd edn. Wiley, Klein DR (1990) Variation in quality of caribou and reindeer forage New York plants associated with season, plant part, and phenology. Rangifer Couturier S, Jean D, Otto R, Rivard S (2004) Demography of the Special 10(3):123–130. https​://doi.org/10.7557/2.10.3.841 migratory tundra caribou (Rangifer tarandus) of the Nord-du- Klein JA, Harte J, Zhao XQ (2007) Experimental warming, not grazing, Québec region and Labrador. Ministère des Ressources naturelles, decreases rangeland quality on the Tibetan Plateau. Ecol Appl de la Faune et des Parcs, Direction de l’aménagement de la faune 17:541–557. https​://doi.org/10.1890/05-0685

1 3 Polar Biology (2019) 42:1561–1570 1569

Krab EJ, Roennefarth J, Becher M, Blume-Werry G, Keuper F, Glob Change Biol 17:3633–3643. https​://doi.org/10.111 Klaminder J, Kreyling J, Makoto K, Milbau A, Dorrepaal E 1/j.1365-2486.2011.02515​.x (2018) Winter warming efects on tundra shrub performance Plante S, Champagne E, Ropars P, Boudreau S, Lévesque E, Trem- are species-specifc and dependent on spring conditions. J Ecol blay B, Tremblay J-P (2014) Shrub cover in northern Nunavik: 106:599–612. https​://doi.org/10.1111/1365-2745.12872​ can herbivores limit shrub expansion? Polar Biol 37:611–619. Leik RK (1997) Experimental design and the analysis of variance. https​://doi.org/10.1007/s0030​0-014-1461-6 Pine Forge Press, Thousand Oaks Pop EW, Oberbauer SF, Starr G (2000) Predicting vegetative bud Lévesque E, Henry GHR, Svoboda J (1997) Phenological and growth break in two arctic deciduous shrub species, Salix pulchra and responses of Papaver radicatum along altitudinal gradients in Betula nana. Oecologia 124:176–184. https​://doi.org/10.1007/ the Canadian High Arctic. Glob Change Biol 3:125–145. https​ s0044​20050​005 ://doi.org/10.1111/j.1365-2486.1997.gcb14​5.x Post E, Forchhammer MC (2008) Climate change reduces reproduc- Linderholm HW (2006) Growing season changes in the last century. tive success of an Arctic herbivore through trophic mismatch. Agric For Meteorol 137:1–14. https​://doi.org/10.1016/j.agrfo​ Phil Trans R Soc B 363:2367–2373. https​://doi.org/10.1098/ rmet.2006.03.006 rstb.2007.2207 Manseau M, Huot J, Crête M (1996) Efects of summer grazing by Post E, Klein DR (1999) Caribou calf production and seasonal range caribou on composition and productivity of vegetation: com- quality during a population decline. J Wildl Manag 63:335–345. munity and landscape level. J Ecol 84:503–513. https​://doi. https​://doi.org/10.2307/38025​17 org/10.2307/22614​73 Post E, Pedersen C, Wilmers CC, Forchhammer MC (2008) Warm- Mårell A, Hofgaard A, Danell K (2006) Nutrient dynamics of ing, plant phenology and the spatial dimension of trophic mis- reindeer forage species along snowmelt gradients at difer- match for large herbivores. Proc R Soc B 275:2005–2013. https​ ent ecological scales. Basic Appl Ecol 7:13–30. https​://doi. ://doi.org/10.1098/rspb.2008.0463 org/10.1016/j.baae.2005.04.005 Ravolainen VT, Bråthen KA, Ims RA, Yoccoz NG, Henden J-A, Marion GM, Henry GHR, Freckman DW, Johnstone J, Jones G, Jones Killengreen ST (2011) Rapid, landscape scale responses in MH, Levesque E, Molau U, Molgaard P, Parsons AN, Svoboda riparian tundra vegetation to exclusion of small and large mam- J, Virginia RA (1997) Open-top designs for manipulating feld malian herbivores. Basic Appl Ecol 12:643–653. https​://doi. temperature in high-latitude ecosystems. Glob Change Biol org/10.1016/j.baae.2011.09.009 3:20–32. https​://doi.org/10.1111/j.1365-2486.1997.gcb13​6.x Ropars P, Boudreau S (2012) Shrub expansion at the forest–tun- Mesinger F, DiMego G, Kalnay E, Mitchell K, Shafran PC, Ebisuzaki dra ecotone: spatial heterogeneity linked to local topography. W, Jović D, Woollen J, Rogers E, Berbery EH, Ek MB, Fan Y, Environ Res Lett 7:015501. https​://doi.org/10.1088/1748- Grumbine R, Higgins W, Li H, Lin Y, Manikin G, Parrish D, Shi 9326/7/1/01550​1 W (2006) North American regional reanalysis. Bull Am Mete- SAS Institute (2012) The SAS system for Windows V9.3. SAS Insti- orol Soc 87:343–360. https://doi.org/10.1175/BAMS-87-3-343​ tute, Cary Messier F, Huot J, Lehenaf D, Luttich S (1988) Demography of the Seastedt TR, Knapp AK (1993) Consequences of nonequilibrium George river caribou herd: evidence of population regulation resource availability across multiple time scales: the tran- by forage exploitation and range expansion. Arctic 41:279–287. sient maxima hypothesis. Am Nat 141:621–633. https​://doi. https​://doi.org/10.14430​/arcti​c1733​ org/10.1086/28549​4 Ministère des Ressources Naturelles et de la Faune (2003) Vegetation Stenseth NC (2002) Climate, changing phenology, and other life Zones and Bioclimatic Domains in Québec. Gouvernement du history traits: Nonlinearity and match-mismatch to the environ- Québec, Québec. https​://mfp.gouv.qc.ca/engli​sh/publi​catio​ns/ ment. Proc Natl Acad Sci USA 99:13379–13381. https​://doi. fores​t/publi​catio​ns/zone-a.pdf. Accessed 29 May 2019. org/10.1073/pnas.21251​9399 Molau U (1997) Responses to natural climatic variation and experi- Street LE, Burns NR, Woodin SJ (2015) Slow recovery of High Arc- mental warming in two tundra plant species with contrasting life tic heath communities from nitrogen enrichment. New Phytol forms: Cassiope tetragona and Ranunculus nivalis. Glob Change 206:682–695. https​://doi.org/10.1111/nph.1326 Biol 3:97–107. https://doi.org/10.1111/j.1365-2486.1997.gcb13​ ​ Sturm M, Schimel J, Michaelson G, Welker JM, Oberbauer SF, 8.x Liston GE, Fahnestock J, Romanovsky VE (2005) Winter bio- Morrissette-Boileau C, Boudreau S, Tremblay JP, Côté SD (2018a) logical processes could help convert arctic tundra to shrubland. Simulated caribou browsing limits the efect of nutrient addi- Bioscience 55:17–26 tion on the growth of Betula glandulosa, an expanding shrub Taillon J, Barboza PS, Côté SD (2013) Nitrogen allocation to species in Eastern Canada. J Ecol 106:1256–1265. https​://doi. ofspring and milk production in a capital breeder. Ecology org/10.1111/1365-2745.12899​ 94:1815–1827. https​://doi.org/10.1890/12-1424.1 Morrissette-Boileau C, Boudreau S, Tremblay JP, Côté SD (2018b) Taillon J, Festa-Bianchet M, Côté SD (2012) Shifting targets in the Revisiting the role of herbivores in the control of shrub expan- tundra: protection of migratory caribou calving grounds must sion in northern Nunavik. Polar Biol 41:1845–1853. https://doi.​ account for spatial changes over time. Biol Conserv 147:163– org/10.1007/s0030​0-018-2325-2 173. https​://doi.org/10.1016/j.bioco​n.2011.12.027 Myers-Smith IH et al (2011) Shrub expansion in tundra ecosystems: Van der Wal R, Madan N, van Lieshout S, Dormann C, Langvatn dynamics, impacts and research priorities. Environ Res Lett. R, Albon SD (2000) Trading forage quality for quantity? Plant https​://doi.org/10.1088/1748-9326/6/4/04550​9 phenology and patch choice by Svalbard reindeer. Oecologia Olofsson J, Oksanen L, Callaghan T, Hulme PE, Oksanen T, 123:108–115. https​://doi.org/10.1007/s0044​20050​995 Suominen O (2009) Herbivores inhibit climate-driven shrub Walker DA, Raynolds MK, Daniels FJA, Einarsson E, Elvebakk A, expansion on the tundra. Glob Change Biol 15:2681–2693. https​ Gould WA, Katenin AE, Kholod SS, Markon CJ, Melnikov ES, ://doi.org/10.1111/j.1365-2486.2009.01935​.x Moskalenko NG, Talbot SS, Yurtsev BA, Team C (2005) The Pau SE, Wolkovich M, Cook BI, Davies TJ, Kraft NJB, Bolmgren circumpolar arctic vegetation map. J Veg Sci 16:267–282. https​ K, Betancourt JL, Cleland EE (2011) Predicting phenol- ://doi.org/10.1111/j.1654-1103.2005.tb023​65.x ogy by integrating ecology, evolution and climate science.

1 3 1570 Polar Biology (2019) 42:1561–1570

Zamin TJ, Côté SD, Tremblay JP, Grogan P (2017) Experimental Publisher’s Note Springer Nature remains neutral with regard to warming alters migratory caribou forage quality. Ecol Appl jurisdictional claims in published maps and institutional afliations. 27:2061–2073. https​://doi.org/10.1002/eap.1590 Zamin TJ, Grogan P (2012) Birch shrub growth in the low Arctic: the relative importance of experimental warming, enhanced nutri- ent availability, snow depth and caribou exclusion. Environ Res Lett 7:034027. https​://doi.org/10.1088/1748-9326/7/3/03402​7

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