Forest Ecology and Management 318 (2014) 359–369
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Light availability and ungulate browsing determine growth, height and mortality of Abies alba saplings Andrea D. Kupferschmid a,b,⇑, Ulrich Wasem b, Harald Bugmann a a b
Forest Ecology, ITES, D-UWIS, ETH Zürich, Switzerland Swiss Federal Institute for Forest, Snow and Landscape Research WSL, Birmensdorf, Switzerland
a r t i c l e
i n f o
Article history: Received 13 November 2013 Received in revised form 20 January 2014 Accepted 21 January 2014 Available online 27 February 2014 Keywords: Mammalian winter herbivory Tree regeneration Survival rates Gap Canopy openness Ground-vegetation competition
a b s t r a c t Ungulate browsing is one of the many factors that affect structure and species composition of forests. Silver fir (Abies alba) is a highly desirable tree species in many European mountain regions, but at the same time one of the most preferred tree species by ungulates. Failure of natural fir regeneration is thus often attributed to browsing. We employ natural light gradients with planted fir saplings but natural browsing to analyze: (i) under which light conditions fir saplings grow and survive best; (ii) where and which ungulate species browse saplings; and (iii) which saplings react and survive best after browsing. The experiment was carried out in a Swiss forest in two fenced plots where parts extended from closed stands into gaps and an unfenced plot under closed canopy. On the three plots 803 fir saplings had been planted in 2008. On half of the total area, browsing had been allowed in at least the winter of 2009/2010. The more light available, the better was the growth of the saplings before and after browsing. For canopy openness P11%, some fir saplings had large height increments irrespective of the exact light level. Video surveillance demonstrated that chamois was the only browsing ungulate species. Mortality was positively correlated with light availability, probably due to site preparation, i.e. mainly where ground vegetation was abundant, and with mouse browsing in one plot. Mortality due to chamois or mice was 2.8–16.4% in plots unfenced for one winter and 52% in the plot unfenced for three winters. A small fraction (10%) of browsed saplings that survived used flagging of a twig to form a new leader, and fully compensated for browsing-related height loss. The other saplings showed a partial compensation in the 2nd year after browsing with equally long shoots, but they still remained shorter than unbrowsed saplings. Saplings under a very dense canopy often did not react (7%). The strong impacts of ungulates on fir recruitment are thus more due to the strong preference of the ungulates for this tree species rather than to a low tolerance of fir to browsing. We do not recommend planting firs in forest gaps due to higher mortality rates, since: (1) competition with ground vegetation is higher in gaps, (2) they risk becoming desiccated and (3) mouse browsing is more likely. Thus we provide evidence that A. alba regeneration benefits from moderately shaded conditions. Ó 2014 Elsevier B.V. All rights reserved.
1. Introduction European silver fir (Abies alba Miller, called ‘fir’ in this paper) is an economically important tree species. Fir plays a role in providing protection from natural hazards like snow avalanches or rockfall in many European mountain forests as it has deep roots and is not very susceptible to insect attack (Frehner et al., 2005). However, fir is among the most preferred tree species for browsing by ungulates such as red deer (Cervus elaphus L.), roe deer (Capreolus ⇑ Corresponding author at: Swiss Federal Institute for Forest, Snow and Landscape Research WSL, Zuercherstr. 111, CH-8903 Birmensdorf, Switzerland. Tel.: +41 79 654 71 78. E-mail address:
[email protected] (A.D. Kupferschmid). http://dx.doi.org/10.1016/j.foreco.2014.01.027 0378-1127/Ó 2014 Elsevier B.V. All rights reserved.
capreolus L.) and chamois (Rupicapra rupicapra L.) (Gill, 1992; Ammer, 1996; Motta, 1996). In the course of a single day, individual mammals – unlike most leaf-eating insects – feed upon several different plant parts and plants. Ungulates tend to browse particular types of trees selectively, i.e., tall, conspicuous saplings appear to be more liable to browsing than small, partially obscured plants (e.g., Reimoser and Gossow, 1996; Kupferschmid et al., 2013). Generally, selective browsing on vigorously growing plants or plant modules (plant vigor hypothesis, Price, 1991) is very common (e.g., Iason et al., 1996). Unbrowsed fir saplings show high morphological plasticity as a function of irradiance (e.g., Grassi and Bagnaresi, 2001). However, fir is a shade-tolerant tree species (Brzeziecki and Kienast, 1994).
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Thus, a light availability of about 10% site openness (Kupferschmid et al., 2013) seems to be sufficient for large terminal shoot increments of fir saplings. Light levels higher than 50% of above canopy light (Stancioiu and O’Hara, 2006), with 30% of canopy openness (Kucˇeravá et al., 2013), and 18% of open-field intensity (Robakowski et al., 2003) were found to rather negatively influence the height increment of fir saplings. Fir saplings thus appear to be also able to grow well under somewhat shaded conditions, e.g. in small gaps (e.g., Muscolo et al., 2010) or under shelterwood (e.g., Kucˇeravá et al., 2013). Once a tree has been browsed, the effect of light on fir growth is less clear. The few published studies can broadly be divided into three groups: trunk cross-sectional analyses of trees from forests, clipping treatments under nursery conditions, and observations of fir saplings often in comparison of fenced vs. unfenced sites. Trunk cross-sectional analyses were carried out at various sites by cutting 1.3 m tall fir trees lengthwise and counting bite marks and sapling age (e.g., Eiberle and Dürr, 1985). The higher age of the browsed saplings compared to unbrowsed ones was interpreted as a growth reduction due to browsing. Based on mortality assumptions (Schreyer and Rausch, 1978), thresholds of ‘acceptable’ annual browsing intensity were calculated for fir saplings between 10 and 130 cm height. They were found to vary between 5.2% and 19% (e.g., Eiberle and Dürr, 1985; Eiberle and Nigg, 1987). The differences in light availability or other site factors may have caused this variability among sites. Clipping experiments with fir in open areas in Switzerland showed that growth varied even more after winter treatment, ranging from substantial decreases to increases in tree height (Eiberle, 1978; Häsler et al., 2008). Kupferschmid and Bugmann (2013) attributed this variability to the variation in sapling vitality, since fast-growing fir saplings overcompensated for the height loss by flagging up a side shoot, while slow-growing saplings had reduced height growth and heights. The timing of the simulated browsing also had a large impact on the response and thus on the height of the saplings at the end of the experiment (Kupferschmid and Bugmann, 2013). Summer browsing was observed to have the most negative effects (Vandenberghe et al., 2008). Repeated clipping also had a negative impact (e.g., Eiberle, 1978). Observational studies based on fenced and unfenced plots have often blamed the lack of natural fir regeneration, at least in higher height classes, on browsing ungulates (Schreyer and Rausch, 1978; Wasem and Senn, 2000). Ammer (1996) found that fir saplings were taller in fenced than unfenced plots under good light conditions, but not in shaded plots and their annual terminal growth was similar in fenced and unfenced plots. The height difference due to heavy browsing by chamois and red deer over a single winter, increased for all fir saplings over the subsequent two years at 10–14% canopy openness (Kupferschmid et al., 2014). In contrast, along light gradients from closed forest stands (approx. 1% canopy openness) to windthrow areas (up to 65% canopy openness), the most vigorously growing fir saplings were browsed, and thus the 3-year growth of the few suppressed unbrowsed saplings was still smaller than that of the browsed saplings regardless of the light level (Kupferschmid et al., 2013). The vitality of a single fir sapling, which depends greatly on its specific environment, affects both the probability that a sapling will be browsed and its reaction after browsing. An experiment with natural browsing along natural light gradients, but with even-aged planted saplings, would enable us to disentangle the effects of (i) the selection of specific saplings by ungulates, and (ii) the differences in individual fir saplings resilience to browsing. We therefore set up an experiment along two natural light gradients from closed forest stands to gaps. A natural light gradient implies a gradient of other abiotic and biotic factors such as soil moisture, nutrient availability, temperature, duration
of snow cover, and competition from ground vegetation. Our specific objectives were to analyze: (i) under which light conditions fir saplings grow and survive best without browsing, (ii) where and which ungulate species browse fir saplings, and (iii) which fir saplings react and survive best after browsing.
2. Methods 2.1. Site The forest ‘Alten Bann’ (coordinates 46° 590 0000 N/9° 050 0700 E) is located above Schwanden (Canton of Glarus, Switzerland) 995– 1020 m above sea level. It has a north-eastern aspect and an inclination of 12–25°. The stand belongs to the Milio-Fagetum typicum (nomenclature of Frehner et al., 2005). Wind storms and scattered bark beetle infestations have caused some small gaps, with a maximum diameter of one tree height. The soil is a humid cambisol with Verrucano and not limestone as bedrock. The humus form is moder, the clay content about 10% and the soil thus rather porous. There was no sign of waterlogging; water storage capacity amounts to only 8 mm in the top 24 cm of the soil and 85 mm for a soil depth of 100 cm. Thus, in spite of 1600 mm precipitation per year (measured in Elm, distance ca. 6 km, MeteoSchweiz 1998–2010), there is a considerable drought risk in the topsoil, particularly after warm dry winds (the so-called ‘Föhn’). Since 1548 AD, the site has been part of the oldest European wildlife sanctuary ‘Freiberg Kärpf’, which covers an area of 102 km2 with about 680 chamois, 173 red deer, 143 roe deer and 90 capricorns in 1997 (Müller and Zopfi, 1999). In recent years, targeted hunting was undertaken to prevent the spread of infectious keratoconjunctivitis among chamois, and to reduce the impacts of wild ungulates to tree regeneration (F. Luchsinger, local wildlife ranger, pers. comm.).
2.2. Experimental design and measurements of environmental variables Two fenced plots parallel to the contour lines were constructed in spring 2008 along a light gradient from closed forest to small gaps. Plot A was 25 m long and 6 m wide, plot B 18 m 6 m (Fig. 1). Both 2 m high fences were split in half along their long axis by a 1 m tall fence, so that the upper part of each fence could be temporarily removed (see browsing experiment below). In the center along the long axis of the resulting 4 fenced parts, we recorded the temperature 5 cm above the soil surface using 2 temperature loggers every ca. 2 m from autumn 2008 to autumn 2011 (Fig. 1). The 80 loggers (DS1921G-F5#, ThermochronÒ iButton 40 °C to 85 °C, maxim integrated) were wrapped in aluminium foil and placed under a small wooden shelter. We were able to calculate the days with deep snow cover for the winters 2008/09, 09/10, and 10/11 by assuming that the daily variation in the measured temperature would be zero on days with significant snow cover. We also calculated the mean temperature for the entire year and for the growing season (April to August) as well as the annual degree-day sum (summation of the days with a mean temperature P5 °C [°C d]). At all temperature measurement points, fish-eye photographs were taken 85 cm above the ground in July 2009. We converted the images to black-and-white using the SideLook software (Nobis, 2005), and calculated the percentage of canopy openness, and the diffuse and direct light for the entire year, for the whole growing season and for just June (cf. Fig. S1) using the software Gap Light Analyzer (Cary Institute of Ecosystem Studies, 1999).
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Fig. 1. Sketch of the site with the three plots (A, B and C). The sketch is not drawn to scale, as horizontal distances are about three-fold compressed. The arrows indicate the position from which the picture of each plot was taken.
Canopy openness was linearly correlated with diffuse light throughout the whole year along both plots (r = 0.998, Fig. S1), and with direct light in plot B (r = 0.88). In plot A, however, direct light was constant for longer than canopy openness (r = 0.38, Fig. S1). The degree-day sum and mean daily temperature for the entire year and for the growing season were only weakly related to direct light (r = 0.47, 0.76, 0.25) and indirect light (r = 0.35, 0.14, 0.46). The number of days with deep snow cover was correlated with diffuse light or canopy openness (r between 0.77 and 0.79), but not with direct light (r between 0.08 and 0.20) in all three years. Plot C was located between the two fenced plots (Fig. 1) and was bordered by large Picea abies trees (distance ca. 8–10 m). Within this plot we placed 8 temperature loggers at four points, each approx. 2–4 m away from a spruce tree, and measured light (for the method, see above). Under this closed canopy, the measured canopy openness was between 7.9% and 10% (cf. Fig. S1).
the gaps, and ground vegetation including tall Polytrichum mosses was weeded in a 2.5 cm radius around each living sapling annually in July. 2.4. Browsing experiment The upper half of plot A and B was opened on 14 October 2009, i.e., two growing seasons after planting, to allow natural browsing by chamois, roe and red deer. Animal activity was monitored using three automatic infrared-sensitive cameras (Moultrie GameSpy I-60, Trailcampro.com) per plot. We closed the fences when most of the terminal shoots of the saplings had been browsed. In plot B, fir saplings were browsed along the whole gradient and the fence was closed on 31 March 2010. In plot A, only the saplings under the canopy had been browsed by that time, and the fence was thus not closed until 20 April 2010. 2.5. Regeneration measurements
2.3. Fir plantation On 13th May 2008, about 665 small 2/0 bare rooted fir saplings were planted in the two plots (A and B) spaced 50 cm apart. The seed came from the Lochwald above Oberhelfenswil (Canton of St. Gallen, 750 m a.s.l., westerly aspect). Where Vaccinium myrtillus, ferns or tussock grasses dominated, the soil was scarified. In the gap of plot A, more competing vegetation was present, and thus more soil preparation had been carried out when planting than under the more shaded conditions and in plot B and C. We planted 20–21 fir saplings around each of the four temperature measurement points in plot C, resulting in a total of 82 saplings, again spaced 50 cm apart. In autumn 2008 and 2009, the tree height (H2008 and H2009), individual annual terminal growth (g2007, g2008, g2009) and side shoot growth were measured on all living fir saplings. This enabled us to calculate the total length of shoots with green needles (s2008, s2009). For dead saplings, the likely cause of death was recorded (see below). Dead saplings were replaced with saplings temporarily placed close to plot C. The replanted saplings were then measured in the same way as the original saplings. Where required, the ground vegetation in plots A and B (not needed in C) was mown around the fir saplings, in particular, in
After closure of the fences but before bud elongation in spring 2010, we measured the remaining tree height (Hbrowsing), the remaining length of the annual growth of the terminal (gbrowsing) and side shoots (used to calculate sbrowsing). Furthermore we noted if the sapling was browsed on the terminal shoot and/or on side shoots. We tried to distinguish between browsing by ungulates (chamois) and mice, as follows. Terminal shoot browsing was attributed to chamois if the browsing injury was ‘‘straight’’ (cf. Fig. S2a), and to mice if it was ‘‘frayed and rough’’ and teeth marks or bark feeding were visible on the stem (cf. Fig. S2b) or when roots were browsed. It was classified as ‘unknown’ if it was angular but without teeth marks (cf. Fig. S2c). We did this also for saplings that were always within the fences (though chamois could not enter these parts of the plots). In addition, we estimated the causes of mortality, i.e., ‘desiccating’, ‘uprooting’, ‘trampling’, ‘browsing’ or ‘missing’. In autumn 2010 and 2011, we measured tree heights (H2010 and H2011), terminal shoot growth (g2010 and g2011) and side shoot lengths (used to calculate s2010 and s2011). We recorded how the sapling had responded two years after terminal-shoot browsing by evaluating the ‘location of reaction’ (i.e., ‘no reaction’, ‘uppermost bud whorl’, or ‘lower bud whorl’) and the ‘reaction type’
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(i.e., ‘terminal shoot’, ‘no reaction’, production of ‘new basal shoot’ out of a bud on a whorl, production of ‘new distal shoot’ out of a bud on the stem or on the remaining terminal shoot pieces and ‘flagging’ of an existing whorl or internodal side shoot). Browsed saplings were then classified into 10 detailed ‘reaction modes’ (Fig. 2). For example, the saplings c, g and k in Fig. 2 all have the reaction type ‘new basal shoot’, but c and g have as the location of the reaction ‘lower bud whorl’, whereas for k this is ‘uppermost bud whorl’. Furthermore, we determined the number of terminal shoots to assess multi-trunking. In addition, all naturally germinated fir seedlings were marked in autumn 2008 through 2011 in plots A and B to individually follow their survival rate. 2.6. Statistical analysis The target variables for all statistical analyses were tree height (H) and the length of the terminal shoot (g) or of all annual shoots (s) prior to browsing (2008 and 2009), directly after browsing (browsing) and one to two vegetation seasons after browsing (2010 and 2011). The environmental variables measured along the long axis of plots A and B were interpolated from the measurement points to every sapling. Then the explanatory variables were grouped into environmental variables (canopy openness, diffuse light and direct light during the whole year or only during the vegetation season or only in June, snow duration, mean daily temperature during the whole year or only during the vegetation season, degree day sum), sapling height (H2008, H2009, Hbrowsing, H2010, H2011), terminal shoot growth (g2007, g2008, s2008, etc.) reaction and browsing (location and type of reaction, reaction mode, browsing, browsing animal). Of each group, only one or, if not correlated at r < 0.5, two to three variable(s) was/were included in the statistical analysis,
so as not to overfit the statistical models with correlated variables (e.g., correlation between light and temperature variables). The plantation time (spring vs. autumn) was also included in the original model but was never significant, and was thus omitted. In special cases, interactions were integrated, e.g., light with reaction type. The target and explanatory variables were transformed using Tukey’s first-aid transformations, i.e., log10(x) for measured data and square root(x) for counted data (Mosteller and Tukey, 1977). The data were analyzed using the procedure lm of the statistical software R (Version 2.15.0, R Development Core Team, 2011) by fitting linear regression models. Insignificant variables were removed from the model. The best candidate models were selected using the lowest value of Akaike’s Information Criterion (AIC), together with the highest AIC weights (similar method to that in chapter 5, Stauffer, 2008). All fir saplings living at the time of the measurements of the target variables were included in the statistical analysis, e.g., all trees living in autumn 2009 when H2009 was analyzed. 3. Results 3.1. Under which light conditions do fir saplings grow best? Height (H2008 and H2009), height increments (g2008 and g2009) and total shoot length (s2008 and s2009) prior to browsing were larger the more light was available (Table S1, Fig. 3a and b). However, variability along the light gradient was high, and above approx. 11% canopy openness (equivalent at our site to 2.2 mols/m2 d diffuse light, Fig. S1), terminal shoot growth was close to its maximum (Fig. 3b). Temperature, in contrast, was negatively related to H2009 (Table S1). Height and/or shoot length in the previous years had a positive effect (Table S1), due to high correlations between height and shoot growth (cf. Fig. 3c).
Fig. 2. Sketches of the reaction modes of Abies alba saplings to browsing in winter 2009/2010. (a) Unbrowsed sapling in autumn 2011, shown as reference. (b) No reaction, (c) basal shoot out of whorl hypocotyl/g07, (d) flagging whorl shoot out of whorl hypocotyl/g07, (e) distal shoot on g07, (f) flagging short shoot out of g07, (g) basal shoot out of whorl g07/g08, (h) distal shoot on g08, (i) flagging short shoot out of g08, (k) basal shoot out of whorl g08/g09, and (l) distal shoot on g09.
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3.2. Under which light conditions do fir saplings survive best? From the 665 fir saplings planted in spring 2008 in the plots A and B, 51 died within half a year, i.e. 7.7% (Table 1). Mortality during this first vegetation season was higher in plot A (10.3%) than in plots B (4.0%) and C (0%, Table 1). In plot A, we found only three dead saplings at a canopy openness below 12%, resulting in a positive relationship between mortality and light until autumn 2008 (Fig. S3). During the first winter and the second vegetation period, mortality in plot A and B was similar (Table 1), and it was more or less evenly distributed over the light gradient (Fig. S3). The main cause of death was desiccation (Table 1). 3.3. Where are fir saplings browsed less often? Half of each fence was opened in winter 2009/2010 to allow browsing by chamois, roe and red deer. The game cameras captured only chamois browsing on saplings, but no roe or red deer.
b
g2009
4 0
5
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H2009
6
15
a
Between 31 March and 20 April 2010, no chamois was filmed in plot A (fence B was already closed at that time), but many holes and galleries of mice were found in April 2010. Thus it is likely that chamois browsed along the entire light gradient in plot B, but in plot A only under the canopy, i.e. they ignored the saplings in the gap (Fig. 3d), probably because there the snow cover lasted longer. Of the saplings exposed to browsing during the winter 2009/2010, 62% were browsed on their terminal shoot in the plots A and B (Table 1). However, in plot A, 53% of the browsing was associated with ‘chamois’, 19% with ‘unknown’ and 28% with ‘mice’, whereas in plot B, the corresponding numbers were 98%, 2% and 0% (Table 1). While no browsing occurred within the fenced part of plot B, mice and unknown animals browsed on 8.4% of the fir saplings in the fenced part of plot A. Thus no saplings that were always enclosed were found to have been browsed by chamois (Table 1). Browsing in winter 2010/2011, when fences A and B remained closed, was negligible (3 saplings, Table 1), and almost no new holes and galleries of mice were found. Thus, mice and chamois browsing occurred during the same winter (i.e., 2009/2010). Apart from terminal shoot browsing, whorl or internodal side shoots were often browsed (Table 1). The drawing in Fig. 2 shows a lightly browsed fir sapling, but many saplings were intensively browsed down to the whorl g2007/g2008 or even deeper, so that no unbrowsed shoot remained (Fig. S2), and many g2009 were missing after browsing. Thus, we decided to analyze the sum of the remaining pieces of g2008 and g2009 as gbrowsing (Table 2) rather than the remaining piece of g2009.
8
In the first autumn after planting, the fir saplings were smaller in plot B than in plot A (H2008 in Table S1), possibly due to deeper planting. The factor ‘plot’ had an influence neither on height one year later, nor on the height increments in all years (Table S1). Sapling height and growth were similar in those part of the plots that were later opened, compared to the parts that remained enclosed, and hence the factor ‘fence’ was dropped out of the statistical models.
8
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d
unfenced - A fenced - A unfenced - B fenced - B
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4 2
g2009
6
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12
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canopy openness
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15
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90
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Fig. 3. Height (H2009) and terminal shoot increment (g2009) prior to browsing (cm) vs. canopy openness (%) or each other (c). Lines indicate simple linear regressions between the two variables. (d) Remaining height (Hbrowsing) in percentage of H2009 (Hbrowsing (%)) for saplings terminally browsed by chamois, unknown animals or mice. Note that Hbrowsing can be higher than H2009 in cases of slight uprooting.
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Table 1 Information on the number of fir saplings from spring 2008 till autumn 2011. Parts of the fences in plots A and B were opened in winter 2009/2010, while plot C was always unfenced. Browsing intensity is the number of fir saplings browsed by ungulates, mice or other mammals on the annual terminal shoot (i.e. the leader growth) within one year as a proportion of the total number of all living saplings. Plot Fence Planting spring 2008 (no. of saplings) Mortality till autumn 2008 Replacement planting autumn 2008 Total alive autumn 2008 Total planted fir saplings
A No 195 29 31 197 226
A Yes 192 11 14 195 206
A Tot 387 40 45 392 432
B No 173 8 8 173 181
B Yes 105 3 3 105 108
B Tot 278 11 11 278 289
Tot A + B Tot 665 51 56 670 721
C No 82 0 0 82 82
Browsing in winter 2008/09 (terminal shoot) Terminal bud damage in winter 2008/09 Total no. of normal growing firs in autumn 2009 Mortality autumn 2008 till autumn 2009: total Cause of death: Desiccation Missing Browsing in winter 2008/2009 Total alive in autumn 2009
0 21 165 11 11 0 0 186
0 15 176 4 3 1 0 191
0 36 341 15 14 1 0 377
0 8 158 7 7 0 0 166
0 5 97 3 3 0 0 102
0 13 255 10 10 0 0 268
0 49 596 25 24 1 0 645
23 4 51 20 4 3 13 62
Browsing in winter 2009/10: terminal shoot Browsing animal: Chamois Unknown Mice Browsing in winter 2009/10: side shoots Mortality autumn 2009 till autumn 2010: total Cause of death: Desiccation Missing Trampling Root feeding Browsing in winter 2008/2009 Browsing in winter 2009/2010 Total alive in autumn 2010
116 62 22 32 29 23 2 1 2 4 0 14 163
16 0 3 13 4 1 0 0 0 0 0 1 190
132 62 25 45 33 24 2 1 2 4 0 15 353
103 101 2 0 47 3 0 0 0 0 0 3 163
0 0 0 0 0 0 0 0 0 0 0 0 102
103 101 2 0 47 3 0 0 0 0 0 3 265
235 163 27 45 80 27 2 1 2 4 0 18 618
45 45 0 0 3 18 1 0 0 0 5 12 44
Browsing in winter 2010/2011: terminal shoot Browsing in winter 2010/2011: side shoots Terminal bud damage in winter 2010/2011 Mortality autumn 2010 till autumn 2011: total Cause of death: Desiccation Browsing in winter 2009/2010 Browsing in winter 2010/2011 Total alive in autumn 2011
2 1 1 18 2 16 0 145
1 3 1 2 1 1 0 188
3 4 2 20 3 17 0 333
0 0 2 2 0 2 0 161
0 0 0 0 0 0 0 102
0 0 2 2 0 2 0 263
3 4 4 22 3 19 0 596
9 1 0 11 1 9 1 33
Browsing intensity in winter 2008/2009 (%) Browsing intensity in winter 2009/2010 (%) Browsing intensity in winter 2010/2011 (%) Mortality spring – autumn 2008 (%) Mortality autumn 2008 – autumn 2009 (%) Mortality autumn 2009 – autumn 2010 (%) Mortality autumn 2010 – autumn 2011 (%) Mortality spring 2008 – autumn 2011 (%) Animal induced mortality 2008–2009 (%) Animal induced mortality 2009–2010 (%) Animal induced mortality 2010–2011 (%) Animal induced mortality 2008–2011 (%)
0.0 62.4 1.2 14.9 5.6 12.4 11.0 35.8
0.0 8.4 0.5 5.7 2.1 0.5 1.1 8.7
22.9
0.0 62.0 0.0 4.6 4.0 1.8 1.2 11.0
0.0 0.0 0.0 2.9 2.9 0.0 0.0 5.6
9.0
0.0 36.4 0.5 7.7 3.7 4.2 3.6 17.3
11.3 9.8 16.4
0.5 0.5 1.5
9.3
1.8 1.2 2.8
0.0 0.0 0.0
1.7
3.9 3.1 6.2
28.0 72.6 20.5 0.0 24.4 29.0 25.0 59.8 15.9 27.4 22.7 52.4
Chamois had usually browsed larger shoot pieces than ‘unknown’ and these in turn than mice (Table 2). Nevertheless, no difference could be found between the plot A and B, and the factor ‘plot’ was therefore dropped from the statistical models of Hbrowsing, sbrowsing and gbrowsing. Overall, the percentages of the remaining heights and shoots were larger with increasing snow duration or higher light availability and the browsing species had no influence on the percentage of the remaining height after browsing (Table 2 and Fig. 3d). As expected, the total length of shoots (sbrowsing) was greater when only the side shoots instead of the side and terminal shoots were browsed (Table 2). In plot C. which had always been unfenced, the browsing intensity during the first winter 2008/2009 amounted to 28.0%, in the second 72.6% but in the third only 20.5%, because a small number of unbrowsed fir saplings remained, i.e., on average 40% (Table 1). Only one out of 82 fir saplings in plot C remained unbrowsed and three had solely side shoot browsing. All the other saplings were browsed at least once on a terminal shoot (5 trees even twice) or had been killed due to browsing (Table 1).
3.4. Under which conditions do fir saplings react best after browsing? Overall, fir saplings that had been browsed on their terminal shoot in winter 2009/2010 were significantly smaller 1–2 years after browsing than those with only side-shoot browsing, and these in turn were smaller than unbrowsed trees (Table 2). However, the new terminal shoot of saplings browsed on the terminal shoot was shorter than that of unbrowsed ones only in the first year after browsing (g2010), while in 2011 they had the same length (g2011, Table 2). This suggests that they partially compensated for height loss already in the 2nd year after browsing. Height 1–2 years after browsing was positively correlated with residual height after browsing (i.e. Hbrowsing, Tables 2–4) and the location of the reaction (Table 3). Saplings that reacted with shoots out of the uppermost remaining whorl or the remaining stem part (‘location of reaction’ uppermost bud whorl) were largest, followed by those 11% of the saplings that reacted with shoots from whorls lower down the stem than the whorl at which browsing occurred (i.e., ‘location of reaction’ lower bud whorl, Table 3). Saplings that
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Table 2 Coefficients of the regression models for height (H), height increment (g) and total shoot length (s) of all living Abies alba saplings in the plots A and B. Target variables for browsed saplings are percentages of the remaining height or shoots in percent of the corresponding values before browsing. The reference for ‘browsing’ is terminal browsing in winter 2009/2010, and for ‘browsing animal’ chamois. Abbreviations: Mean temperature during vegetation season (Temp), adjusted R-squared (R2). Intercept
Direct lighta
Snow coverb
Tempa
Degree day suma
Hbrowsinga
Browsing Side shoots
Analysis for browsed Hbrowsinga gbrowsing2008 + 2009b sbrowsinga
saplings 15.11 4.92*** 53.21***
Analysis for all living saplings H2010a 0.18*** H2011a 0.23*** g2010c 1.35*** g2011c 2.53*** s2010c 7.66*** s2011c 4.59***
9.49* 4.45*** –
5.27***
0.07*** 0.14*** 0.26*** 0.24*** 0.13* 0.21***
0.03*** 0.04*** 0.07*** 0.11*** 0.14*** 0.12***
–
–
Browsing animal No
–
8.30***
17.71*** – – – 1.24** – 2.73***
– – – – 1.72*** –
0.88*** 0.87*** 0.65*** 0.58*** 1.32*** 1.62***
0.14*** 0.08*** 0.50*** 0.11*** 0.57*** 0.29***
Unknown
Mouse
– 2.68*** 5.85
– 2.38*** 11.25***
0.16*** 0.12*** 0.58*** -0.02 0.85*** 0.40***
R2
Df
0.11 0.18 0.36
2/216 3/215 4/293
0.90 0.84 0.78 0.46 0.78 0.72
5/560 5 / 541 5/534 6/529 6/547 6/531
a
Data log-transformed. Data square-root transformed. c Data log-transformed but saplings with no reaction were omitted. *** p 6 0.001. ** p 6 0.01. * p 6 0.05. p 6 0.1 (insignificant trend). b
had not formed a new terminal shoot two years after browsing (‘no reaction’, approx. 7% of all browsed saplings) tended to be smaller before browsing (H2009), and were definitely shorter directly after browsing (Hbrowsing) or in the following years than other saplings (Fig. 4, Table 3). However, the location of the reaction did not affect their height increment after browsing in both years (Table 3). If we integrate the detailed ‘reaction mode’ (Fig. 2) into the statistical model for height 1–2 years after browsing, it is striking that height after browsing follows almost exactly the stem height of the reaction (Table 4): fir saplings that reacted from the whorl hypocotyl–g2007 (Fig. 2c) were smallest, followed by those that reacted with a distal bud on g2007 (Fig. 2e), and then those that reacted with
a basal bud out of the whorl g2007/g2008 (Fig. 2g), and so on. The largest trees were those that reacted with a distal bud on the remaining stem part of g2009 (Fig. 2l, Table 4). Flagging of a side shoot from a whorl was rare and occurred only out of the lowest whorl (hypocotyl–g2007, Fig. 2d), probably due to the strong browsing not only of the terminal but also of the side shoots (cf. Fig. S2). However, saplings reacting with flagging of a whorl or internodal side shoot (Fig. 2d, f, and i) were larger and had significantly longer new terminal shoots in 2010 than would be expected from the stem height of the reaction (cf. Table 4). Flagging was clearly the most successful type of reaction 1–2 years after browsing. In a statistical model with only browsed
Table 3 Coefficients of the regression models for height (H) and height increment (g) of all living Abies alba saplings in the plots A and B. The reference for ‘location of reaction’ is ‘no reaction’, and for ‘reaction type’ flagging. ‘No reaction’ is only included in reaction type if the factor ‘location of reaction’ is not in the model. The types of reactions (‘flagging’ (cf. Fig. 2d, f, and i), ‘basal shoot’ (Fig. 2c, g, and k), ‘distal shoot’ (Fig. 2e, h, and l), ‘terminal shoot’ (Fig. 2a) and ‘no reaction’ (Fig. 2b)) are defined in the text. H2010a
0.079 0.248*** 0.151*** 0.855***
0.218 0.845*** 0.949 1.291***
0.346 1.196*** 0.598*** 1.271***
Location of reaction Uppermost bud whorl Lower bud whorl
0.175*** 0.131***
0.219* 0.123**
– –
– –
0.115*** 0.126*** 0.046*
0.132*** 0.112*** 0.007
0.681*** 0.812*** 0.336** 1.369*** 0.388 1.227* 0.372 1.221.
0.224 0.163 0.197 1.710***
0.905 8/538
0.841 8/538
0.795 11/535
0.513 7/539
lighta lighta lighta lighta
to to to to
*
new basal shoot new distal shoot normal terminal shoot no reaction
Data log-transformed. Data square-root transformed. p 6 0.001. ** p 6 0.01. * p 6 0.05. p 6 0.1 (insignificant trend). ***
g2011b
0.000 0.172*** 0.074*** 0.876***
Adjusted R-squared Df a
g2010b
Intercept Diffuse lighta Direct lighta Hbrowsinga
Type of reaction Basal shoot Distal shoot Terminal shoot No reaction Interaction direct Interaction direct Interaction direct Interaction direct
b
H2011a
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Table 4 Coefficients of the regression models for the height (H) and height increment (g) of living Abies alba saplings in the plots A and B that had been browsed in winter 2009/2010. The reference for ‘reaction mode’ is ‘no reaction’ (Fig. 2b), unless ‘ref.’ is mentioned. H2010a *
Intercept Diffuse lighta Direct lighta Hbrowsinga Reaction mode Basal out of hypocotyl/g07 Flagging out of hypocotyl/g07 Distal on g07 Flagging short shoot out of g07 Basal out of g07/g08 Distal on g08 Flagging short shoot out of g08 Basal out of g08/g09 Distal on g09 Adjusted R-squared Df
Fig. 2 c d e f g h i k l
H2011a ***
g2010b
g2011b ***
0.085 0.274*** 0.060** 0.723***
0.238 0.305*** 0.113*** 0.624***
0.732 1.103*** 0.374*** -
0.144 0.865*** 0.245*** -
0.038 0.125* 0.003 0.088* 0.050* 0.051 0.149* 0.086*** 0.087**
0.122** 0.167** 0.021 0.079 0.068* 0.096** 0.176* 0.142*** 0.199***
Ref. 0.653** 0.238 0.403* 0.190 0.241 0.710** 0.335** 0.202
Ref. 0.226 0.113 0.131 0.118 0.231* 0.320 0.314** 0.433***
0.832 12/174
0.825 12/174
0.394 10/158
0.451 10/165
a
Data log-transformed. Data log-transformed but saplings with no reaction were omitted as the height increment g was zero. *** p 6 0.001. ** p 6 0.01. * p 6 0.05. p 6 0.1 (insignificant trend). b
Fig. 4. Height prior to browsing (H2009), directly after browsing (Hbrowsing), and height (H2010 and H2011) and height increment (g2010 and g2011) 1–2 years after browsing in plots A and B, separately for the different types of reaction of all living Abies alba saplings. The types of reaction (‘flagging’ (cf. Fig. 2d, f, and i), ‘basal’ (Fig. 2c, g, and k), ‘distal’ (Fig. 2e, h, and l), ‘terminal’ (Fig. 2a) and ‘no shoot’ (Fig. 2b)) are defined in the text. The width of the boxes represents the number of trees reacting with each type.
saplings, the 23 browsed fir saplings (10%) that reacted with flagging had longer terminal shoots in 2010 (g2010) and were thus taller in 2010 (H2010) than the 147 fir saplings that reacted with a basal shoot (64%) or the 44 saplings that reacted with a distal shoot (19%, Table 3). Furthermore, while saplings that reacted with flagging had smaller height increments one year after browsing than unbrowsed saplings (g2010), they were only slightly shorter than
unbrowsed ones in autumn 2010 (H2010) as the flagged side shoot compensated for the browsed piece (Table 3, Fig. 4). In 2011, all browsed saplings that had formed a new terminal shoot had height increments (g2011) similar to those of unbrowsed saplings (Table 3 and Fig. 4). This led to similar H2011 for unbrowsed saplings and browsed saplings that reacted with flagging (Table 3 and Fig. 4). The few fir saplings that used flagging of a whorl or internodal side
A.D. Kupferschmid et al. / Forest Ecology and Management 318 (2014) 359–369
shoot thus compensated for the browsing-related height loss after a singular browsing event. The other browsed fir saplings (83%) showed partial compensation in the 2nd year after browsing, but they were still significantly shorter than unbrowsed saplings (Table 3 and Fig. 4), albeit with a high variability (Fig. S4). The more light a sapling received or the longer the snow cover, the taller were the fir saplings 1–2 years after exposure to ungulate browsing, regardless of whether they had been browsed or not (Table 2–4, Figs. 3 and S4). This raises the question whether individual types of reactions were more frequent under particular light conditions. In the statistical model for g2010 (i.e. one year after browsing), the interaction ‘direct light reaction type’ was significantly negative for fir saplings that responded with shoots from distal buds or which did not react, unlike that for saplings that used flagging (Table 3). It can therefore be concluded that saplings under a dark canopy often did not react at all or with distal buds on lower parts of the stem. Flagging, in contrast, occurred along the whole light gradient (Fig. S4), but tended to be more frequent with more light (cf. the negative interaction coefficients of all other types of reaction in Table 3). Many of the surviving fir saplings that had been browsed on their terminal shoot had not only one but several new terminal shoots two years after browsing (Table S2). Only 4% of the unbrowsed saplings were forked, while 25% of the terminally browsed saplings were forked and 6% were multi-stemmed. About one third of the multiple stems grew out of the deepest whorl, i.e. the hypocotyl–g2007. This multi-stemming was independent of light availability. 3.5. Under which conditions do fir saplings survive best after browsing? No statistical analysis was made due to the very small number of dead saplings per year, per plot and per cause of death (cf. Table 1). The mortality of the fir saplings was greater in plot A than in plot B, both before and after browsing (Table 1). Overall, from planting in spring 2008 to autumn 2011, mortality amounted to 36% in the partially unfenced part of plot A, while it was distinctly smaller in the fenced parts of plot A and both parts of plot B (Table 1). In the partially unfenced part of plot A, animals were the cause of about half of the total sapling mortality from the time of planting in spring 2008 to autumn 2011, but only 25% of the mortality in the partially unfenced part of plot B (Table 1). However, while mortality from autumn 2009 to autumn 2010 (including the winter with browsing) tended to be more frequent when more light was available, this was not the case from autumn 2010 to autumn 2011 (Fig. S3). Of the 82 fir saplings planted in plot C, 33 survived until 2011, i.e. the total sapling mortality amounted to 60% in the continuously unfenced plot C (Table 1). Of this, chamois browsing was responsible for at least 88% of the total sapling mortality, resulting in an average annual mortality induced by browsing of 22% (Table 1). All saplings with fewer than three green needles remaining after browsing on the stem died immediately. 3.6. Natural establishment of fir seedlings Natural regeneration was generally very rare in plot A, i.e. only 3 seedlings germinated from natural seed fall in autumn 2010. In plot B, one seedling was found in autumn 2008 and one in autumn 2009. However, in autumn 2010, 110 seedlings from natural seed fall were found, i.e. 1.2 seedlings/m2. In autumn 2011, 15 more seedlings were found. The mortality of the seedlings that germinated in 2010 was 14.5% during the first winter (both parts of plot
367
B were fenced at that time). The cause of their mortality could not be determined, as most seedlings were missing in 2011.
4. Discussion 4.1. Under which conditions do fir saplings survive best with and without browsing? Site conditions had an influence on the mortality rate of fir saplings in our experiment, i.e. mortality tended to be more frequent when more light was available. Where abundant ground vegetation had been removed to prepare the site for planting in gap A, the fir saplings more frequently became desiccated. This scarification thus may have influenced the mortality rate, albeit in a counter-intuitive manner. The upper soil layer in such sites had a low water storage capacity that probably decreased further due to site preparation. Thus drought risk was high, particularly after warm-dry winds. Natural establishment of seedlings occurred only in plot B, but not in plot A. Near our fences, the sown fir germinated and survived better under a 2 mm mesh net than without, probably because it changed the environmental conditions, creating more humidity (Wasem and Senn, 2000). However, overly wet conditions are also unfavorable, as the one-year survival of fir seedlings was only 3% in sinkholes and 84% on the edge of an elevated plain (Tan and Bruckert, 1992). Generally, the establishment of fir was found to benefit from moderately humid conditions or, conversely, fewer dry periods (e.g., Muscolo et al., 2010; Kupferschmid et al., 2013) and strong competition from ground vegetation led to higher fir seedling mortality in places where the site had not been prepared (Szymura et al., 2007). Although the browsing intensities in plots A and B when the fences were open were similarly high (62%), not only the base mortality but also the percentage of animal-induced mortality was around twice as high in plot A than in plot B (Table 1). In plot A, mice probably benefited from the site preparation and the mowing of the ground vegetation in the gap part, as mowing has been found to stimulate mouse browsing (Odermatt and Wasem, 2004). In a clipping experiment in the Jura Mountains, vole predation (5%) was a more important cause of fir sapling death than the clipping treatment (2%, cf. Tan and Bruckert, 1992). In extreme cases, mice can lead to 10–50% failure (Odermatt and Wasem, 2004) or even 100% mortality (Bäumler and Hohenadl, 1980) in fir plantations. In our case, mouse browsing was frequent in one winter only (the winter when we opened parts of the fences) and thus clearly did not reach such high levels. However, total mortality tended to be higher, at least in some years, the more light was available, probably due to site preparation and mouse browsing. In contrast, the annual mortality in plot B was higher in the years before fence opening (2008–2009) than during (2009– 2010) or afterwards (2010–2011), and was always lower than 5% (Table 1) and thus almost negligible. In a study by Motta (1996), the lethality of browsing was nil where ungulate densities were low, but increased with greater ungulate densities. We converted the ungulates counted in the ungulate sanctuary to which our site belongs (Müller and Zopfi, 1999) to UDI (Ungulate Density Index) and DDI (Deer Density index = red deer density + l/5 roe deer density per 100 ha) according to Motta’s (1996) approach. The resulting UDI = 3.9 and DDI = 2 are low values according to Motta (1996). Vandenberghe et al. (2008) found that clipping reduced fir sapling survival by 2%, while the presence of neighbors reduced it by about 5% from June to September one year later. In another study, losses due to browsing were also uncommon (Pépin et al., 2006), which suggests that the influence of occasional ungulate
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browsing on tree seedlings is more closely related to growth reduction than to induced mortality. Where browsing by ungulates was allowed in every year under closed canopy conditions in our experiment (i.e., in plot C), the annual browsing intensity was 40% and chamois browsing was responsible for at least 88% of the total sapling mortality. Animal induced mortality was therefore clearly higher than the compensatory mortality of fir regeneration in dark stands and thus has an effect for the long-term forest development. In the Bavarian Alps with a browsing intensity of about 75%, 60% of the unfenced fir saplings were already dead under the closed canopy after one year (Ammer, 1996). The total fir sapling mortality over 20 years was about 98% under a closed canopy and 70% in a heavy shelterwood, while mortality inside fenced areas were 20% and 50%, respectively (Ammer, 1996). In the long term, continuous browsing by ungulates caused there approx. 78% and 20% of the mortality. Eiberle (1989) postulated for fir and Norway spruce saplings that annual browsing intensities of 10%, 20% and 30% cause 4.6%, 40% and 75% mortality, respectively. Browsing-induced mortality in our plot C was thus for the moment lower than that estimated by Eiberle (1989) and that found under the closed canopy in the Bavarian Alps (Ammer, 1996). However, only one sapling at our plot C remained unbrowsed, and thus mortality due to past and future browsing will continue and probably lead to a complete failure of fir regeneration. Additional evidence for this is that trials at the same site showed that while sown and planted fir saplings have survived within the fence, none at all remain outside the fence (Wasem and Senn, 2000). This suggests that the ungulate impact can be extremely high, even though the ungulate density is ‘low’. A minimum of needles have to be present to enable fir saplings to survive and react after browsing. Evergreen coniferous tree species mostly store their reserves in needles, in contrast to deciduous species that store them preferentially in stems and roots (cf. Millard et al., 2001). The minimum of needles and thus of reserves might be lower for young and small saplings (such as those in our experiment) than for taller saplings (such as in Kupferschmid et al., 2014). This supports the recommendation to integrate into browsing assessments the tree vitality and the ‘‘feeding-strength’’ – i.e. buds, fraction of or whole annual terminal shoots, all annual shoots, or more than the annual shoots. 4.2. Where are fir saplings browsed less often? In our study site only chamois, and no red and roe deer browsed on our saplings, although at least some red deer did browse the tall unfenced fir saplings in the same period (cf. Kupferschmid et al., 2014). Larger saplings are probably more attractive for roe and red deer. Moreover roe deer may have avoided the site during winter because of the presence of the other ungulate species and deep snow cover. Browsing by chamois was more frequent under canopy than in gaps with snow cover as in plot A. Snow can sometimes protect small saplings from ungulate browsing, especially if browsing is mainly restricted to winter and spring, which seems to be often the case for fir saplings in Switzerland (Odermatt, 2014). However, it is particularly these ‘safe sites’ with snow cover, where mice browsed on shoots and roots. As a result, browsing was uniformly distributed across the light gradient. Shoot browsing by mice was less intensive than browsing by chamois, but mice probably induced more sapling mortality (see above). Studies in Sweden and Norway indicate that reindeer and, in particular, vole herbivory influenced the vegetation more in open heathlands than in forests. This implies that intense and localised selective foraging by small mammals may have a more marked effect on vegetation than transient feeding by reindeer (Olofsson et al., 2006). In Switzerland,
both saplings and seedlings were prone to browsing by deer and rodents under high levels of diffuse light, while with increasing levels of direct light, deer were less likely to browse saplings (Häsler, 2008). This again indicates that the level of browsing on small firs is also related to mice and vole abundance, in particular where much light is available. At our site, chamois browsing occurred every year (cf. plot C) along the whole light gradient (cf. plot B) whereas mice browsing occurred only once locally in plot A. 4.3. Under which conditions do fir saplings grow and react best? The more light available, the higher were the fir saplings prior to browsing and 1–2 years after browsing. However, the variability in height along the light gradient was large, and fir sapling height increments larger than 6 cm were already found with approx. 11% canopy openness (Fig. 3). The light level was similar when we analyzed natural fir regeneration at several other sites in Switzerland (Kupferschmid et al., 2013). An important feature of our experiment is that the ground vegetation around the small saplings was mown every June, thus minimizing aboveground competition with ground vegetation. Such treatment is not usual in normal silviculture in Swiss mountain forests. Thus ground vegetation may further hamper the growth and survival of fir saplings in gaps. Full compensation for the height loss induced by browsing was observed in about 10% of the saplings along the whole light gradient, i.e. even under a completely closed canopy (Fig. S4). In clipping experiments, flagging was more frequent under full light conditions (cf. Häsler et al., 2008). In contrast, flagging rarely occurred in natural fir regeneration at different sites with roe deer browsing regardless of the light conditions (Kupferschmid et al., 2013). In another experiment at our site, no tall fir sapling showed flagging, which could be simply attributed to very intensive browsing (Kupferschmid et al., 2014) or to potential additional genetic differences. However, our results indicate that flagging can occur in Swiss mountain forests even under dark conditions if unbrowsed internodal or whorl side shoots remain after browsing and the saplings have a high morphological plasticity. In contrast, the two reactions ‘no reaction’ in the first 2 years after browsing and ‘new shoots out of distal buds’ on the lower parts of the stem were both more abundant the more shaded the sapling environment was. Delayed reactions seem to be common for fir saplings (Osterloher and Wiechmann, 1993), in particular under shaded conditions (Häsler et al., 2008) and after insect or frost impacts in dark stands (Kupferschmid et al., 2013). Thus, a minimum canopy openness of about 11% enhances not only the growth prior to and after browsing, but also influences sapling’s reactions after browsing. Four out of five browsed fir saplings that survived reacted with partial compensation in the second year after browsing, i.e. they formed terminal shoots equal in length to those in unbrowsed saplings (Fig. 4). However, the height loss induced by browsing and the shorter shoots in the first year after browsing resulted in these saplings remaining shorter than unbrowsed saplings, as many other studies have also found (e.g. Welch et al., 1992). About one third of the browsed trees became forked or multistemmed, as found in many other studies (e.g. Långström and Hellqvist, 1992). However, on most multi-stemmed saplings, the strongest vertical shoot becomes dominant while the others degenerate into side shoots (Welch et al., 1992; Bergquist et al., 2003). 5. Conclusion We provide strong evidence that A. alba regeneration benefits from moderately shaded conditions due to: (i) lower mortality
A.D. Kupferschmid et al. / Forest Ecology and Management 318 (2014) 359–369
(although in gaps this depends probably on site preparation to reduce the abundant ground vegetation and how much browsing by mice occurs), (ii) the good growth development of fir saplings with as little as 11% canopy openness, (iii) the delayed reaction to browsing under very dark canopies (i.e., no reaction until 2 years after browsing), (iv) the flagging of side and internodal shoots to compensate for browsing independent of light levels, and (v) the sensitivity of seedling establishment to dry periods. This confirms the competitive advantages of fir regeneration under moderately shaded conditions as suggested in other studies (e.g. Muscolo et al., 2010; Kucˇeravá et al., 2013). The fact that small fir saplings reacted to browsing surprisingly well with even full compensation in 10% of the saplings and that the chamois-induced mortality was high with repeated browsing suggest that the impacts of browsing on fir sapling survival, and the often observed failure of fir regeneration, are probably due to the strong preference of the ungulates for this tree species, rather than to a low browsing tolerance of fir. Acknowledgments We are grateful to A. Tschudi and H. Mariacher from the municipality of Glarus Süd for their help with fence construction and other competent assistance. We thank A. Burkart (WSL, Birmensdorf, Switzerland) for support with seeds and seedlings, A. Siegfried for field help in 2010 and the analysis of the fish-eye photos, S. Zimmermann and M. Walser (WSL) for help with the soil profile and soil analysis, A. Schwyzer (WSL) for painting the reaction types in Fig. 2, S. Dingwall for language revision, and a forest practitioner advisory group for their discussions and comments. The work of the first author was funded by the Swiss Federal Office for the Environment through the project ‘Langfristige Walddynamik unter Ungulaten-Einfluss’, Contract No. 00.0138.PZ/H362-1153. Appendix A. Supplementary material Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.foreco.2 014.01.027. References Ammer, C., 1996. Impact of ungulates on structure and dynamics of natural regeneration of mixed mountain forests in the Bavarian Alps. For. Ecol. Manage. 88, 43–53. Bäumler, W., Hohenadl, W., 1980. Über den Einfluß alpiner Kleinsäuger auf die Verjüngung in einem Bergmischwald der Chiemgauer Alpen. Forstw. C.bl., vol. 99, pp. 207–221. Bergquist, J., Bergström, R., Zakharenka, A., 2003. Responses of young Norway spruce (Picea abies) to winter browsing by roe deer (Capreolus capreolus): effects on height growth and stem morphology. Scan. J. For. Res. 18, 368–376. Brzeziecki, B., Kienast, F., 1994. Classifying the life- history strategies of trees on the basis of the Grimian model. For. Ecol. Manage. 69, 167–187. Cary Institute of Ecosystem Studies, 1999. Gap Light Analyzer (GLA). In: Simon Fraser University. Institute of Ecosystem Studies. . Eiberle, K., 1978. Folgewirkungen eines simulierten Wildverbisses auf die Entwicklung junger Waldbäume. Schweiz. Z. Forstwes. 129, 757–768. Eiberle, K., 1989. Über den Einfluss des Wildverbisses auf die Mortalität von jungen Waldbäumen in der oberen Montanstufe. Schweiz. Z. Forstwes. 12, 1031–1042. Eiberle, K., Dürr, C., 1985. Grenzen der Verbissbelastung für die Weisstanne (Abies alba) in der kollinen Stufe. Waldhygiene 16, 95–106. Eiberle, K., Nigg, H., 1987. Grundlagen zur Beurteilung des Wildverbisses im Gebirgswald. Schweiz. Z. Forstwes. 183, 747–785. Frehner, M., Wasser, B., Schwitter, R., 2005. Nachhaltigkeit und Erfolgskontrolle im Schutzwald. Wegleitung für Pflegemassnahmen in Wäldern mit Schutzfunktion. Bundesamt für Umwelt, Wald und Landschaft, Bern. Gill, R.M.A., 1992. A review of damage by mammals in north temperate forests: 1. Deer. Forestry 65, 145–169. Grassi, G., Bagnaresi, U., 2001. Foliar morphological and physiological plasticity in Picea abies and Abies alba saplings along a natural light gradient. Tree Physiol. 21, 959–967.
369
Häsler, H., 2008. Impact of browsing by wild ungulates on growth and regeneration of European silver fir. Doctoral Thesis, Diss. ETH No. 17911. Zürich: University of Zürich. Häsler, H., Senn, J., Edwards, P.J., 2008. Light-dependent growth responses of young Abies alba to simulated ungulate browsing. Funct. Ecol. 22, 48–57. Iason, G.R., Duncan, A.J., Hartley, S.E., Staines, B.W., 1996. Feeding behaviour of red deer (Cervus elaphus) on sitka spruce (Picea sitchensis): the role of carbon– nutrient balance. For. Ecol. Manage. 88, 121–129. Kucˇeravá, B., Dobrovolny´, L., Remeš, J., 2013. Responses of Abies alba seedlings to different site conditions in Picea abies plantations. Dendrobiology 69, 49–58. Kupferschmid, A.D., Bugmann, H., 2013. Timing, light availability and vigour determine the response of Abies alba saplings to leader shoot browsing. Eur. J. For. Res. 132, 47–60. Kupferschmid, A.D., Wasem, U., Bugmann, H., 2014. Ungulate browsing leads to height and diameter growth reduction on Abies alba saplings planted along light gradients. Eur. J. For. Res., accepted for publication. Kupferschmid, A.D., Zimmermann, S., Bugmann, H., 2013. Browsing regime and growth response of naturally regenerated Abies alba saplings along light gradients. For. Ecol. Manage. 310, 393–404. Långström, B., Hellqvist, C., 1992. Height growth recovery and crown development in top-damaged Pinus sylvestris trees. Scand. J. For. Res. 7, 237–247. Millard, P., Hester, A.J., Wendler, R., Wendler, B., 2001. Interspecific defoliation responses of trees depend on sites of winter nitrogen storage. Funct. Ecol. 15, 535–543. Mosteller, F., Tukey, J.W. (Eds.), 1977. Data Analysis and Regression: A Second Course in Statistics. Addison-Wesley, Reading. Motta, R., 1996. Impact of wild ungulates on forest regeneration and tree composition of mountain forests in Western Italian Alps. For. Ecol. Manage. 88, 93–98. Müller, P., Zopfi, P., 1999. Vom Wildschutz zum Naturschutz. In: 450 Jahre Freiberg Kärpf. Verlag Neujahrsbote, Linthal, pp. 11–17. Muscolo, A., Sidari, M., Bagnato, S., Mallamaci, C., Mercurio, R., 2010. Gap size effects on above- and below-ground processes in a silver fir stand. Eur. J. For. Res. 129, 355–365. Nobis, M., 2005. SideLook 1.1 – imaging software for the analysis of vegetation structure with true-colour photographs. . Odermatt, O., 2014. Zu welcher Jahreszeit werden Bäume verbissen? Wald Holz February. Odermatt, O., Wasem, U., 2004. Mäuseschäden bei der Wiederbewaldung von Windwurfflächen. In: waldwissen.net. BFW, FVA, LWF, WSL, WSL, Schweiz. Olofsson, J., Hulme, P.E., Oksanen, L., Suominen, O., 2006. Importance of large and small mammalian herbivores for the plant community structure in the forest tundra ecotone. Oikos 106, 324. Osterloher, A., Wiechmann, R., 1993. Verbissbelastung durch Schalenwild: Zur unterschiedlichen Verbisstoleranz der Baumarten. Allg. Forstztg. (Wien) 22, 1159–1160. Pépin, D., Renaud, P.-C., Boscardin, B.Y., Goulard, M., Mallet, C., Anglard, F., Ballon, P., 2006. Relative impact of browsing by red deer on mixed coniferous and broadleaved seedlings – an enclosure-based experiment. For. Ecol. Manage. 222, 302– 313. Price, P.W., 1991. The plant vigor hypothesis and herbivore attack. Oikos 62, 244– 251. R Development Core Team, 2011. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. . Reimoser, F., Gossow, H., 1996. Impact of ungulates on forest vegetation and its dependence on the silvicultural system. For. Ecol. Manage. 88, 107–119. Robakowski, P., Montpied, P., Dreyer, E., 2003. Plasticity of morphological and physiological traits in response to different levels of irradiance in seedlings of silver fir (Abies alba Mill.). Trees 17, 431–441. Schreyer, G., Rausch, V., 1978. Der Schutzwald in der Alpenregion des Landkreises Miesbach. Bayerisches Staatsministerium für Ernährung, Landwirtschaft und Forsten. Stancioiu, P.T., O’Hara, K.L., 2006. Regeneration growth in different light environments of mixed species, multiaged, mountainous forest of Romania. Eur. J. For. Res. 125, 151–162. Stauffer, H.B., 2008. Contemporary Bayesian and Frequentist Statistical Research Methods for Natural Resource Scientists. John Wiley & Sons, Inc., Hoboken, New Jersey. Szymura, T.H., Dunajski, A., Aman, I., Makowski, M., Szymura, M., 2007. The spatial pattern and microsites requirements of Abies alba natural regeneration in the Karkonosze Mountains. Dendrobiology 58, 51–57. Tan, B.S., Bruckert, S., 1992. Effect of physical environmental factors on the initial stages of the natural regeneration of fir (Abies alba) at some sites in the Jura. Ann. Sci. For. 49, 337–349. Vandenberghe, C., Freléchoux, F., Buttler, A., 2008. The influence of competition from herbaceous vegetation and shade on simulated browsing tolerance of coniferous and deciduous saplings. Oikos 117, 415–423. Wasem, U., Senn, J., 2000. Fehlende Weisstannenverjüngung: Hohe Schalenwildbestände können die Ursache sein. Wald Holz 9, 11–14. Welch, D., Staines, B.W., Scott, D., French, D.D., 1992. Leader browsing by red and roe deer on young Sitka spruce trees in western Scotland. II. Effects on growth and tree form. Forestry 65, 309–330.
Supplementary Material / Appendix: Table S1: Coefficients of the regression models for height (H), terminal shoot growth (g) and total shoot length (s) of living Abies alba saplings prior to browsing. Significance codes: *** p ≤ 0.001, ** p ≤ 0.01, * p ≤ 0.05 and . p ≤ 0.1 (insignificant trend). Intercept
a
Degree a day sum
0.66 *** 0.13 **
0.08 ***
a 2009
1.90 *** 0.24 ***
0.09 *** -0.54 ** 0.37 *** 0.17 ***
H
s
Direct a light
a 2008
H
g
Diffuse a light
a 2009
a 2009
-0.05
0.99 ***
0.49 *** 0.23 **
Data log-transformed
-
a
a
g2007
a
H2008
s2008
0.15 ***
Plot B
Adjusted R-squared
Df
-0.04 **
0.26 4 / 591
0.66 *** 0.13 ***
-
0.78 5 / 590
-
-
-
0.25 2/ 593
-
0.86 ***
-
0.27 3/ 592
-
Table S2: Number of terminal shoots of all living Abies alba saplings in plots A and B prior and 1 to 2 years after browsing, and occurrence of multi-stemming. period 2009 2010
2011
browsing 09/10 none none terminal shoot side shoot none terminal shoot side shoot
number of terminal shoots 1 2 3 639 6 0 316 6 0 187 26 5 75 3 0 306 13 0 137 51 13 73 2 1
total living [N] 645 322 218 78 319 201 76
multi-stemmed [%] 0.9 1.9 14.2 3.8 4.1 31.8 3.9
2.5
3.0
3.5
1500 1450 1350
1400
degree day sum
13.0 12.5
mean daily temperature 1.5
2.0
2.5
3.0
3.5
1.5
2.0
diffuse light
2.5
3.0
3.5
1.5
3.0
3.5
1500 degree day sum
13.0 12.5
1350
mean daily temperature
12.0
120
snow cover duration
2.5 diffuse light
8
80
90 100
16 14 12 10
2.0
diffuse light
140
diffuse light
1450
2.0
1400
1.5
canopy openness
12.0
120
snow cover duration
90 100 80
10
12
14
16
unfenced - A fenced - A unfenced - B fenced - B unfenced - C
8
canopy openness
140
0.5
1.0
1.5
2.0
direct light
2.5
3.0
0.5
1.0
1.5
2.0
direct light
2.5
3.0
0.5
1.0
1.5
2.0
direct light
2.5
3.0
0.5
1.0
1.5
2.0
2.5
3.0
direct light
Fig. S1: Diffuse and direct light [Mols m-2 d-1] vs. canopy openness [%], mean daily temperature during the growing season in 2009 [°C], degree day sum in 2009 [°C*d], and snow cover duration [d] in winter 2008/2009 [d].
a)
game
b)
mouse
c) ?
Fig. S2: Browsing by chamois, mice or marked as unknown (?) because the angular browsing injury was without teeth marks.
mortality 2009
10 8 4
6
H2008 [cm]
2.0 1.5
unfenced - A fenced - A unfenced - B fenced - B
0.5
2
1.0
direct light [Mols*m-2*d-1]
2.5
12
3.0
14
mortality 2008
alive
0 8
10
12
14
16
8
10
canopy openness [%]
mortality 2011 mouse
15
H2010 [cm]
5
5
10
10
H2009 [cm]
20
15
25
unknown
16
30
20
chamois
14
canopy openness [%]
mortality 2010 unbrowsed
dead 2009 12
10
side shoot browsed
12 canopy openness [%]
dead 2010
14
16
dead 2011
0
0
terminal shoot browsed
8
8
10
12
14
16
canopy openness [%]
Fig. S3: Light influence on Abies alba sapling mortality in plots A and B. Top left: saplings that died between planting in spring and autumn 2008. Top right: saplings that died between autumn 2008 and autumn 2009 (black cross) in contrast to living saplings (grey circles). Bottom left: saplings that died in 2010 (black) in comparison to unbrowsed saplings (unfilled circles), and saplings with terminal (dark grey) or side-shoot browsing (light grey) by chamois (square), unknown (diamond) or mice (triangle). Black triangles filled white indicate the few saplings with root browsing by mice. Bottom right: similar to bottom left, but for saplings that died in 2011.
Fig. S4: Light dependence of the height (H2010 and H2011) and height increment (g2010 and g2011) of all living Abies alba saplings 1-2 years after browsing in plots A and B. The types of reaction (‘flagging’ (cf. Fig. 2d, f, i), ‘basal’ (Fig. 2c, g, k), ‘distal’ (Fig. 2e, h, l), ‘terminal’ (Fig. 2a) and ‘no’ reaction (Fig. 2b)) are defined in the text.
