Growth, Nutrient Content, Fruit Production and Herbivory in Bilberry Vaccinium Myrtillus L

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Growth, nutrient content, fruit production and herbivory in bilberry Vaccinium myrtillus L. along an altitudinal gradient Downloaded from https://academic.oup.com/forestry/article/77/3/213/527815 by guest on 24 September 2021

I.C. FERNÁNDEZ-CALVO AND J.R. OBESO*

Dpto Biología Organismos & Sistemas, Unidad Ecología, Universidad de Oviedo, E-33071 Oviedo, Spain * Corresponding author. E-mail: [email protected]

Summary Growth, fruit production and herbivory by ungulates in bilberry were investigated in 29 localities from three temperate habitats (oak forest, birch forest and heath) distributed along an altitudinal gradient from 750 to 2000 m a.s.l. Plant height, current year growth and damage by herbivores were influenced by altitude. The herbivory by ungulates increased with altitude inside the woodlands, but had moderate effect in the heaths despite their higher altitude. Furthermore, when only oak forest sites were considered, nitrogen content in both twigs and leaves significantly increased with altitude, and nitrogen content in twigs was significantly related to the percentage of shoots affected by ungulate herbivory. Contrarily, the herbivory was reduced in sites exhibiting higher content of acid detergent fibre in leaves. Patterns of fruit production per habitat and altitude were not consistent between years; however, fruit set within the oak forests decreased with increases in the percentage of shoots affected by herbivory. Possible effects of ungulate herbivores on nitrogen concentration of bilberry and its quality as food for herbivorous and frugivorous animals are discussed.

Introduction negative relationship between nitrogen concentration and the temperature of the current year is Altitudinal gradients determine not only temper- a characteristic of some plants (Chapin and ature gradients but also the depth of the snow Oechel, 1983; Haukioja et al., 1985; Laine and and the timing of snow melt which strongly inﬂu- Henttonen, 1987). This inverse relationship may ences plant phenology and the length of the be attributed to a dilution of nitrogen by the growing season (Heegaard, 2002). Both factors increased amount of structural tissue that grows may affect patterns of plant growth, survival, in a warm year, favourable for photosynthesis. reproduction and interactions with herbivores On the other hand, grazing by herbivores (Crawley, 1989). Temperature may also affect the might affect nitrogen content and Danell and nitrogen concentration of vegetation and conse- Huss-Danell (1985) found that leaves from quently its quality as food for herbivores. A experimentally browsed birch contained more

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nitrogen than control leaves. Similarly, Oksanen found (Tolvanen et al., 1993a; Hautala et al., et al. (1987) found that nitrogen concentration in 2001; Frak and Ponge, 2002). bilberry showed the highest levels on the most The main questions that we asked were as intensely grazed localities. However, cause and follows: effect are not clear in these cases because herbivores may select the richest areas. 1 Are there effects of the altitude and habitat on The bilberry (Vaccinium myrtillus L.), a dwarf plant characteristics? shrub, is included in the diet of rodent herbivores 2 Does the effect of ungulate herbivores differ (mainly in Arctic environments) and some wild among habitats and altitudes? (roe deer, red deer) and domestic ungulates 3 Does food quality of bilberry vary with habitat (cattle). Its twigs, leaves and fruits are among the and altitude? main food items of the capercaillie (Tetrao uro- 4 Do fruit traits, production and presentation gallus L.) (Storch, 1993, 1995) and its fruits form (aggregation or dispersion indexes) vary Downloaded from https://academic.oup.com/forestry/article/77/3/213/527815 by guest on 24 September 2021 a large fraction of brown bear (Ursus arctos L.) among altitudes and habitats? diet during the summer (Welch et al., 1997). Several studies have considered the food quality of bilberry as a factor that might explain population changes in herbivore populations (Laine Study sites, materials and methods and Henttonen, 1987; Selas, 2000). The quality Study sites of this species as food for herbivores may be determined, to some extent, by nitrogen concen- The sample sites were located at the Somiedo tration, because total phenolic content, which Natural Park, Asturias Province, northern Spain. might negatively affect herbivore preferences, Thirty study sites were selected in 1998 along an follows opposite patterns to nitrogen content altitudinal gradient between 750 and 2000 m (Laine and Henttonen, 1987). Its quality as food a.s.l. (43º 7′ N, 6º 20′ W in the middle of the for frugivorous animals depends on both fruit study area), including 10 sites at each of the three size and fruit production. Spatial aggregation of vegetation types: oak forests (Quercus petraea fruits is also important for frugivorous animals (Matthuschka) Lieb.), birch forests (Betula because their bite rate is largely determined by celtiberica Rothm. et Vasc.) and heaths of heather berry size, density and distribution within the (Calluna vulgaris (L.) Hull). One heath site was patch (Welch et al., 1997). burnt and was not included in the sampling Altitudinal gradients provide an excellent design during 1999. The sites were distributed in opportunity to examine the effect of temperature separate forest fragments located in three on plant growth and chemical composition. The adjacent valleys (Figure 1) and the mean altitudes work described here investigated the effects of an were 1062 ± 162 m for oak forests, 1437 ± 125 m altitudinal gradient on bilberry performance, for birch forests and 1856 ± 68 m for heaths. growth, fruit production, and herbivory. At the Valley was included as a random factor in the same time we considered the effect of the gradient analyses but was found to be not signiﬁcant. on nitrogen content of bilberry leaves and twigs. The main herbivores on bilberry at these sites The altitudinal gradient was located in the were cattle Bos taurus L., red deer (Cervus Cantabrian range (northern Spain) where elaphus L.) and brown bear (Ursus arctos L). bilberry occurs in a variety of habitats from sea Herbivory by roe deer (Capreolus capreolus L.). level to above 2000 m a.s.l. Here we take into was less important, due not only to their smaller account three different habitats, determined by size and abundance but also to their habitat the vegetation type, where bilberry is the selection and food preferences mainly based on dominant plant in the undergrowth, and which herbaceous plants (Fandos et al., 1987). are distributed at different altitudes: oak forests (lower altitudes), birch forests (middle altitudes) Sampling procedure and heaths of heather (higher altitudes). Besides the effect of the temperature gradient, an effect of At each study site, density of ramets (number of the habitat is expected, as has been previously ramets m–2), plant height (cm), shoot growth 04 cph024 (to/d) 1/6/04 3:48 pm Page 215

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Figure 1. Map of the Somiedo Natural Park including the study sites, forest fragments and rivers.

during 1998 (mm) and presence of herbivory these shoots during summer and the ratio of fruits were determined in 25 randomly selected 60 to flowers calculated. 60 cm quadrats per study site during the spring At each oak forest site shoots and leaves of the of 1999. In each of these quadrats the number of current-year growth from at least four ramets ramets was counted, the height of the shrubs was were sampled for nutrient analysis. All current- measured in two ramets from the soil to the year growth was sampled irrespective of the largest shoot, shoot growth measured in four length and oven dried at 60ºC to constant weight. shoots unaffected by herbivory, and the Acid detergent fibre (ADF), neutral detergent presence–absence of herbivory by ungulates fibre (NDF) and caloric content (cal g–1) were determined on four shoots, which amounts to determined according to the method of Van Es 100 shoots per site. To avoid dependence and Van Der Meer (1980), Van Soest (1963) and between these variables ramets and shoots were Van Soest and Robertson (1980), respectively. randomly selected for each measure. A mean Nitrogen concentration was determined by com- value was obtained for each site and variable. bustion using a standard automated CNH pro- Fruit production was evaluated in summer cedure (PE 2400 SERIES II, CNHS/O). Duplicate (June–September) using 120 small quadrats (25 subsamples of a single bulked sample of several 25 cm) per site in 1998 and 80 quadrats per site plants per locality were analysed and the concen- in 1999. The results of the individual quadrats trations expressed as percentages of dry weight. were employed to calculate the ratio variance to mean as an index of fruit dispersion by site (Greig- Statistical analysis Smith, 1986). Fruit set was estimated in the oak forest sites during 1999 by counting the number Generalized linear models with binomial error and of flowers on 20 shoots marked with plastic tape a log link function (GLIM 3.77) were used to at each site. Fruit production was evaluated in estimate the effect of the factor habitat and the 04 cph024 (to/d) 1/6/04 3:48 pm Page 216

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variables altitude, plant height, current year growth, ramet density and their interactions on the probability of damage by herbivores. Deviances from the model were scaled with the scaled deviance/degrees of freedom to correct for the effects of over-dispersion. GLIM models with binomial error were also used to determine the effect of nitrogen content of leaves and shoots, NDF content, caloric content, current year growth and altitude on the probability of herbivore damage within the oak forests. When the depen- dent variables followed a normal distribution, as is the case of plant height, current year growth, crop Downloaded from https://academic.oup.com/forestry/article/77/3/213/527815 by guest on 24 September 2021 size and mean fruit weight, generalized linear models were calculated using ANCOVA. The models were calculated using sequential tests. To choose the most parsimonious model Akaike’s information criterion (Akaike, 1973) was calculated. After the selection of the model, non-significant sources of variation and non- significant parameters were removed from the models. Parameter estimates were used to determine whether the levels of the factor habitat differed significantly from one another (parameter estimates for birch forest and heaths are actually differences from mean values of oak forests), and when two levels did not significantly differ new levels grouping together the two levels were created to obtain new estimates of the parameters (Crawley, 1993). Only significant parameters were included in the models. In some cases the variable altitude suggested possible quadratic effects (Figures 2 and 3), then the quadratic transformation of altitude was examined in the models (Crawley, 1993). When the transformed variable retained more deviance than the untransformed one, the former was included in the model.

Results Plant height was signiﬁcantly affected by habitat type and altitude; the effect of altitude was

Figure 2. Plant height, shoot growth during 1998 and percentage of bilberry shoots affected by ungulate herbivores (percentage herbivory) at different altitudes in the three habitats studied (oak forests, ﬁlled circles; birch forests, open circles; heaths, triangles). 04 cph024 (to/d) 1/6/04 3:48 pm Page 217

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negative and the height of bilberry plants in birch found for the influence of these variables on forests was higher than in the other habitats current year shoot growth, which were signifi- (Tables 1 and 2; Figure 2). Similar effects were cantly affected by habitat type and altitude. Altitude had a negative effect on plant growth and plants grew more in birch forests than in oak 1000 forests and heaths (Tables 1 and 2; Figure 2). 1999 Altitude, plant height, habitat type and the -2 800 interaction of habitat and altitude had a signifi- 600 cant effect on the proportion of shoots damaged by herbivores (Tables 1 and 3). There was a qua-

umber m 400 dratic effect of altitude on herbivory (Figure 2). The estimates of the interaction terms show that 200 the incidence of herbivory in relation to altitude Downloaded from https://academic.oup.com/forestry/article/77/3/213/527815 by guest on 24 September 2021 Fruit n 0 varied among habitats, increased with altitude within the oak forests and decreased with altitude 400 800 1200 1600 2000 Altitude (m) in the birch forests and heaths (Table 3; Figure 2). Plant height had a negative effect on the percentage of shoots being damaged by herbivores 60 (Table 3).

99 (mg) Fruit production in 1999 was signiﬁcantly 50 inﬂuenced by habitat type and the extent of her-

ht 19 bivore damage. Oak forests produced significantly 40 more fruits than heaths and birch forests (Table 1; Figure 3). However, when the detrimental effect of herbivory on fruit production is removed, par- 30 ameter estimates show that adjusted means for fruit production were lower for heaths than for Fruit dry weig 20 oak and birch forests (Table 4). Similarly indi- 400 800 1200 1600 2000 vidual fruit weight in 1999 was significantly influ- Altitude (m) enced by habitat type and altitude (Tables 1 and 4). When the negative effect of altitude was Figure 3. Mean fruit production (fruits m–2) and removed, adjusted means for birch forests were individual fruit dry weight (mg) in 1999 at different smaller than for other habitats (Table 4; Figure 3). altitudes in the three studied habitats (oak forests, In 1998, individual fruit production was not filled circles; birch forests, open circles; heaths, tri- significantly affected by any independent variable angles). (Table 1) and fruit dry weight within oak forests

Table 1: Mean ± SD (N) values for variables measured in the three different habitats

Oak forests Birch forests Heaths

Number of ramets m–2 132.8 ± 54.3 (10) 69.9 ± 10.7 (10) 236 ± 81.9 (9) Plant height (cm) 30.83 ± 10.85 (10) 35.95 ± 7.18 (10) 21.53 ± 4.42 (9) Shoot growth (cm year–1) 6.44 ± 1.17 (10) 6.94 ± 0.85 (10) 5.01 ± 0.73 (9) Herbivory (%) 46.00 ± 34.22 (10) 81.51 ± 10.20 (10) 19.39 ± 15.14 (9) Dispersion index (1998) 4.17 ± 2.40 (9) 4.99 ± 3.33 (10) 10.51 ± 7.71 (10) Fruit dry weight (g, 1998) 0.044 ± 0.055 (8) 0.034 ± 0.077 (6) 0.040 ± 0.066 (10) Fruits m–2 (1998) 23.4 ± 25.2 (10) 22.1 ± 25.1 (10) 60.1 ± 51.4 (10) Dispersion index (1999) 17.19 ± 8.42 (9) 15.40 ± 19.11 (10) 12.03 ± 11.0 (9) Fruit dry weight (g, 1999) 0.049 ± 0.0005 (9) 0.027 ± 0.006 (9) 0.027 ± 0.006 (9) Fruits m–2 (1999) 350.1 ± 294.7 (10) 84.9 ± 103.2 (10) 153.6 ± 159.7 (9) 04 cph024 (to/d) 1/6/04 3:48 pm Page 218

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Table 2: ANOVA tables and models for the inﬂuence of altitude and habitat on plant height and current year growth Plant height

Source of variation d.f. Deviance FP

Altitude 1 725.3 15.621 <0.001 Habitat 2 797.3 8.586 0.001 Error 25 1160.8 Total 28 2683.4

Parameter Estimate SE

Oak forests 49.53 5.365 Downloaded from https://academic.oup.com/forestry/article/77/3/213/527815 by guest on 24 September 2021 Altitude –0.03538 0.0060 Birch forest and heaths 18.24 4.320

Current-year growth

Source of variation d.f. Deviance FP

Altitude 1 12.680 16.153 <0.001 Habitat 2 9.490 6.045 0.007 Error 25 19.628 Total 28 41.798

Parameter Estimate SE

Oak forests and heaths 8.540 0.7133 Altitude –0.001931 0.0004759 Birch forest 1.179 0.3427

Non-signiﬁcant levels for the factor habitat were grouped to obtain parameter estimates, which represent differences from the parameter estimate for oak.

was greater than within birch forests (F(2,21) = affected by herbivory (r = 0.816; P = 0.013; N = 3.877, P = 0.037). 8; Figure 4). According to dispersion indexes, bilberry fruits Within oak forests, nitrogen content in leaves were distributed in aggregates in most of the sites and shoots, NDF content in leaves, altitude and during both study years (Table 1); however, they current year growth had a significant effect on the were significantly more aggregated in the heaths proportion of shoots damaged by herbivores. than the other habitats in 1998 (F(2,26) = 4.417, P Damage by herbivores increased with altitude, = 0.022). Dispersion indexes were correlated current year growth and nitrogen content of with fruit production (r = 0.856; P < 0.001, N = shoots and decreased with nitrogen content and 29 in 1998; r = 0.550; P = 0.002; N = 28 in NDF in leaves (Table 5; Figures 2 and 4). 1999). However, the effect of herbivores was not When only oak forest sites were considered, related to nitrogen content in leaves (r = 0.214; P nitrogen content in both twigs and leaves signifi- = 0.581; N = 9) and decreased significantly when cantly increased with altitude (r = 0.870; P = ADF in leaves increased (r = – 0.809; P = 0.015; 0.005; N = 8 for twigs and r = 0.706; P = 0.010; N = 8). NDF and caloric content of leaves and N = 8 for leaves; Figure 4). Nitrogen in twigs was twigs were not significantly related to herbivory significantly related to the percentage of shoots intensity. 04 cph024 (to/d) 1/6/04 3:48 pm Page 219

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Table 3: ANOVA table and model for the explanation of the percentage of shoots damaged by herbivores

Source of variation d.f. Deviance FP

Altitude 1 7.778 7.778 0.011 Habitat 2 61.820 30.910 <0.001 Habitat altitude 2 14.470 7.240 0.004 Plant height 1 7.748 7.478 0.011 Residuals 22 22.000 Total 28 113.55

Parameter Estimate SE

Oak forests –1.488 0.5268 Downloaded from https://academic.oup.com/forestry/article/77/3/213/527815 by guest on 24 September 2021 Altitude 2.978 exp (–6) 3.166 exp (–7) Birch forests 7.052 0.6232 Heaths 6.916 1.376 Plant height –0.07076 0.007513 Altitude birch forests –3.697exp (–6) 3.762 exp (–7) Altitude heaths –4.538 exp (–6) 4.936 exp (–7)

A quadratic transformation was applied to the variable altitude; the error distribution was binomial and the residuals were scaled. Parameter estimates are differences from the parameter estimate for oak.

Mean fruit set during 1999 in the oak forests ability in the heaths. In central European forests, was 0.61 ± 0.13 (N = 9) and signiﬁcantly total ground cover and vegetation height of increased with fruit production (r = 0.868, P = bilberry are negatively correlated with tree 0.002) and shoot growth during 1998 (r = 0.791; canopy cover, and bilberry is best in stands of P = 0.011) and decreased with percentage of moderate canopy cover around 50 per cent shoots affected by herbivory (r = –0.841, P = (Storch, 1993, 1995). Similarly, Mäkipää (1999) 0.004) and percentage of nitrogen content in concluded that the relative abundance of Vac- twigs (r = –0.792; P = 0.019). cinium species is controlled by light conditions or moisture availability rather than by nutrients. In fact, Karlsson (1987) found that there is no simple relationship between plant performance Discussion and leaf nitrogen concentration in bilberry. The present study shows that variables related to The herbivory by ungulates increased with plant performance, herbivory and fruit produc- altitude inside the oak woodlands, but decreased tion were signiﬁcantly affected by habitat and at higher altitudes and hence had a moderate altitude. However, we should take into account effect on the heaths. It is not possible to know that the effect of altitude and habitat cannot be whether herbivores increase the amount of properly distinguished because they are not inde- nitrogen in the plants they feed on or if they select pendent variables, the oak forests are at lower the sites according to nitrogen concentration. altitude, the heaths sites are at high altitude and Oksanen et al. (1987) also found that the sites birch forests are intermediate. Our results with intense herbivory by rodents showed the showed that plant height and current year growth highest nitrogen concentration in bilberry plants. decreased with altitude. Furthermore, this indi- Nevertheless, in the study area, the incidence of cates that plants grew less and were relatively herbivory by ungulates in forest habitats was shorter at the oak forest and heath sites, probably probably determined by the presence of adjacent due to reduced light availability within oak pastures, which are more abundant at higher alti- forests and to reduced humus and moisture avail- tudes. Similarly, the fact that herbivory incidence 04 cph024 (to/d) 1/6/04 3:48 pm Page 220

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Table 4: Model for the explanation of bilberry fruit production (number of fruits m–2) and fruit size (individual fruit dry weight, mg) during 1999 Number of fruits m –2

Source of variation d.f. Deviance FP

Herbivory 1 296472 10.968 0.003 Altitude 1 7206 0.258 0.616 Habitat 2 472872 8.747 0.001 Error 23 641502 Total 27 1418052

Parameter Estimate SE Downloaded from https://academic.oup.com/forestry/article/77/3/213/527815 by guest on 24 September 2021

Herbivory –6.278 1.208 Oak and birch forests 959.0 156.3 Heaths –341.8 83.58

Individual fruit dry weight

Source of variation d.f. Deviance FP

Altitude 1 2033.0 67.55 <0.001 Habitat 2 545.0 9.05 0.001 Habitat altitude 2 193.8 3.22 0.060 Residuals 21 632.0 Total 26 3403.3

Parameter Estimate SE

Altitude –0.02487 0.002753 Oak forest and heaths 74.35 4.167 Birch forests –11.28 2.053

ANOVA table was obtained considering that the error distribution was normal. Non-signiﬁcant levels of the factor habitat (oak and birch forests for fruit production and oak forests and heaths for fruit dry weight) were grouped to obtain parameter estimates.

decreased in sites with higher acid detergent ﬁbre tural tissue in the lower localities because the might be either indicative of site selection by her- shoot growth is limited by altitude. bivores or an effect of increased proportion of We can argue that the increase in nitrogen indigestible material as a response to herbivory. content with altitude within the oak forests may We have considered nitrogen content just in the be due to herbivory. Bilberry exhibits a capacity oak forests, assuming that differences attributed to recover after ungulate herbivore damage, to vegetation and soils were not important within especially when current-year branches are the same type of forest. A decrease of nitrogen removed because apical dominance is broken and availability with altitude is expected because of this activates bud development and compen- lower mineralization rates at lower temperatures. satory responses (Tolvanen et al., 1992). Vegeta- Nevertheless, we found an inverse relationship tive recovery of this species has been also between nitrogen content and temperature, demonstrated after experimental spring and associated to the altitudinal gradient, which summer frost (Tolvanen, 1997). When simulated might be attributable to a dilution of similar herbivory is performed early in the growing nitrogen pool sizes by increased amount of struc- season, clipping has a detrimental effect on 04 cph024 (to/d) 1/6/04 3:48 pm Page 221

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Table 5: Model for the explanation of herbivory damage (percentage of damaged shoots) in the oak forests taking into account variables of nitrogen content

Variable d.f Deviance P

Nitrogen in leaves 1 16.332 <0.001 Nitrogen in shoots 1 158.0 <0.001 FND leaves 1 39.4 <0.001 Altitude 1 14.31 <0.001 Current year growth 1 9.292 <0.002 Residuals 2 1.4922 Total 7 238.78

Parameter Estimate SE Downloaded from https://academic.oup.com/forestry/article/77/3/213/527815 by guest on 24 September 2021

Intercept –14.14 2.871 Nitrogen in leaves –2.464 0.5625 Nitrogen in shoots 10.40 2.103 FND leaves –0.1445 0.03549 Altitude 0.005526 0.001413 Current year growth 0.6953 0.2265

The distribution error was binomial and the scale parameter was close to 1.

biomass production (Tolvanen et al., 1994), growth decreasing with later time of clipping (Tolvanen et al., 1993a). Regrowth after herbivory during the current-year growth season means a delay in shoot growth and consequently a greater dependence on translocatable fraction of nitrogen stored in the rhizomes and probably higher protein concentration. The greatest proportion of nitrogen in bilberry tissues is always in the form of proteins and protein concentration is higher in youngest shoots (Lähdesmäki et al., 1990b). This is the way ungulate herbivores may affect nitrogen concentration in bilberry. Moderate herbivory could produce more branches and more biomass in affected plants in the second year after the herbivory damage than in control plants; however, besides direct damage on ﬂowers, fruits and seeds during current year, fruit production will decrease in the following years (Tolvanen et al., 1993b). Then high herbivory levels could have a detrimental effect on the quality of bilberry patches for frugivorous animals. Fruit set in bilberry is pollen limited (Jacque- mart and Thompson, 1996; Jacquemart 1997;

Figure 4. Nitrogen content as percentage of dry weight in twigs (ﬁlled circles) and leaves (open circles) of bilberry from oak forests at different altitudes and at sites with different incidence of herbivory. 04 cph024 (to/d) 1/6/04 3:48 pm Page 222

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but see Fröborg, 1996), so it is possible that However, it remains a challenge to determine altitude constrains pollinator abundance and whether this pattern is determined by herbivory consequently fruit set. However, in the oak itself or rather is an effect of the altitudinal forests studied the effect of altitude was weak and gradient. There is a need for experiments exclud- herbivory, which increased with altitude, had an ing herbivores at different altitudes to reveal the obvious detrimental effect on fruit set. We found effect of both variables in the nitrogen content of that sites showing higher fruit set also exhibited this species. larger shoot growth during the previous growth season. Acknowledgements While Elle (1996) found that reproductive trade-offs were not apparent in the American We thank Alberto Fernández for his help during field cranberry Vaccinium macrocarpon, Tolvanen work, Alfredo Nicieza, Gary Kerr and one anonymous and Laine (1997) documented a positive relation- referee for comments on the manuscript. Analyses of Downloaded from https://academic.oup.com/forestry/article/77/3/213/527815 by guest on 24 September 2021 ship between current-year growth and reproduc- fibre and energy content were made at CIATA, Princi- tion at branch level in bilberry. However, the pado de Asturias. CNH analyses were made by Esteban Cabal. Financial support was obtained from the Prin- absence of this trade-off might also be an effect cipado de Asturias, project SV-PA-97-007, and from of herbivory, which has a detrimental effect on the Ministerio de Ciencia y Tecnología, project MCYT- both fruit set and shoot growth. Sites with higher BOS2000-0451. fruit production also showed the lower nitrogen concentration. Pakonen et al. (1988) and Lähdesmäki et al. (1990a) described a similar References phenomenon at shoot level in bilberry, reporting Akaike, H. 1973 Information theory and the extension that sterile shoots always show higher protein of the maximum likelihood principle. In Inter- concentrations than fertile ones, which may be a national Symposium on Information Theory, 2nd consequence of allocation of protein reserves to edn. B.N. Petran and F. Csaki (eds). Akademiai, flowering and berry production in these latter Budapest, pp. 267–281. shoots. Chapin, F.S. III and Oechel, W.C. 1983 Photosynthesis, respiration and phosphate absorption by Carex Fruit production decreased with altitude in aquatilis ecotypes along latitudinal and local 1999; but neither altitude nor habitat signifi- environmental gradients. Ecology 64, 743–751. cantly affected fruit production in 1998. Fruit Crawley, M.J. 1989 Insect herbivores and plant popu- production was extremely variable between sites lation dynamics. Ann. Rev. Entomol. 34, 531–564. within heaths, despite their narrow altitudinal Crawley, M.J. 1993 GLIM for Ecologists. Blackwell range. Furthermore, heaths showed higher fruit Science, Oxford. aggregation than other habitats in 1998 which Danell, K. and Huss-Danell, K. 1985 Feeding by insects might increase the efficiency of frugivorous and hares on birches earlier affected by moose foraging in this habitat. However, neither altitude browsing. Oikos 44, 75–81. nor habitat affected the aggregation of bilberry Elle, E. 1996 Reproductive trade-offs in genetically distinct clones of Vaccinium macrocarpon, the fruits during 1999. Berry aggregation depended American cranberry. Oecologia 107, 61–70. on fruit production and the crops varied between Fandos, P., Martínez, T. and Palacios, F. 1987 Estudio study years. Fluctuations in berry production at sobre la alimentación del corzo (Capreolus capreo- intervals of 3–5 years seem habitual in this lus L., 1758) en España. Ecología 1, 161–175. species (Selas, 1997) and the closely related Vac- Frak, E. and Ponge, J-F. 2002 The influence of altitude cinium corymbosum shows biennial fluctuations on the distribution of subterranean organs and (Vander Kloet and Cabilio, 1984, 1996). These humus components in Vaccinium myrtillus carpets. fluctuations in berry availability lead to inter- J. Veg. Sci. 13, 17–26. annual variations in the quality of bilberry Fröborg, H. 1996 Pollination and seed production in patches for frugivorous animals. five boreal species of Vaccinium and Andromeda (Ericaceae). Can. J. Bot. 74, 1363–1368. Our results showed that, when the effect of Greig-Smith, P. 1986 Quantitative Plant Ecology, 3rd altitude was removed, the patterns of growth of edn. Blackwell Scientific Publications, Oxford. bilberry varied among habitats. Within the oak Haukioja, E., Niemelä, P. and Sirén, S. 1985 Foliage forests, herbivory, nitrogen content and probably phenols and nitrogen in relation to growth, insect food quality of bilberry increased with altitude. damage, and ability to recover after defoliation, in 04 cph024 (to/d) 1/6/04 3:48 pm Page 223

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