Yew (Taxus Baccata L.) Regeneration Is Facilitated by Fleshy-Fruited Shrubs

Biological Conservation 95 (2000) 31±38 www.elsevier.com/locate/biocon

Yew (Taxus baccata L.) regeneration is facilitated by ¯eshy-fruited shrubs in Mediterranean environments

Daniel GarcõÂ a, Regino Zamora *, JoseÂ A. HoÂ dar, JoseÂ M. GoÂ mez, Jorge Castro

Grupo de EcologõÂa Terrestre, Departamento de BiologõÂa Animal y EcologõÂa, Facultad de Ciencias, Universidad de Granada, E-18071 Granada, Spain

Received 18 August 1999; received in revised form 7 December 1999; accepted 1 February 2000

Abstract Yew Taxus baccata is catalogued as a species endangered and prone to extinction in the Mediterranean mountains of southern Spain, due to the small size and senescent status of most populations. In this paper, we study the eects of herbivory and the protective role of woody shrubs in the regeneration ability of the yew in the Sierra Nevada. The estimated density of the yew in the study plot was 287.9 individuals/ha, more than 90% being juveniles (seedlings and saplings), which were mostly located under ¯e- shy-fruited shrubs. Saplings suered serious herbivore damage when unprotected by shrubs. Thus, ¯eshy-fruited shrubs proved to be the best habitat for seedling establishment and sapling survival and growth. The abundance of ¯eshy-fruited shrubs in our study site provides a yew population characterized by an active regeneration under natural conditions. We suggest that the maintenance of healthy populations of yew in Mediterranean mountains is strongly dependent on the conservation of well-developed ¯eshy-fruit understories and their community of avian dispersers. # 2000 Elsevier Science Ltd. All rights reserved. Keywords: Herbivory on seedlings and saplings; Mediterranean environments; Plant±plant facilitation; Population regeneration; Yew Taxus baccata

1. Introduction of most populations and, consequently, yew has been catalogued as endangered and prone to extinction in Yew (Taxus baccata L., Taxaceae) is a long-lived these areas (HernaÂ ndez and Clemente, 1994). native tree species widely distributed throughout Eur- Natural regeneration of the yew in temperate latitudes ope but declining sharply over most of its range (Tit- appears limited by both seed-predator pressure and the tensor, 1980; Hulme, 1996, and references therein). In scarcity of microsites for recruitment (Hulme, 1996, the Mediterranean Basin, as happens with other plant 1997; Wilson et al., 1996). Moreover, yews are fre- species of boreo-alpine origin (Bennett et al., 1991; Cox quently damaged by vertebrate herbivores despite the and Moore, 1993; GarcõÂ a et al., 1999), this species is foliage being strongly poisonous (Tittensor, 1980; Alli- restricted to the mountain areas, following the climatic son, 1990a, b; Font Quer, 1995). Under herbivore pres- regression after the last Ice Age. As a result of climate sure, juvenile yews bene®t from the protective role of change and human disturbance over centuries, yew dis- nurse plants which mechanically defend yews from tribution in the Mediterranean Basin is formed by a browsers. This idea has been supported by the relation- reduced number of small isolated patches, populations ship between the development of prickly shrublands as a being located mainly in shady ravines on northern seral stage prior to the establishment of well-developed montane slopes (Franco, 1986). In Andalusia (southern yew populations in Great Britain (Watt, 1926; Titten- Spain), yew populations are small, most with less than sor, 1980; Hulme, 1996). 10±20 individuals, and dominated by senescent indivi- The possible dependence of yews on facilitative nurse duals, with a very low proportion of saplings and seed- shrubs to regenerate might be even more evident in lings. These data imply an apparent regeneration failure Mediterranean environments, characterised by high ungulate pressure and strong summer drought, both being factors which limit natural regeneration of many boreal- * Corresponding author. Fax: +34-958-243-238. origin woody species [drought for Abies pinsapo (Arista,

1994) and Juniperus communis (GarcõÂ a et al., 1999); 2.2. Habitat structure ungulate herbivory for Pinus sylvestris var. nevadensis (HoÂ dar et al., 1998)]. In this paper, we analyse the Habitat structure and vegetation coverage were sam- eects of herbivores and the potential protective role of pled in the study area by means of 10 linear 50-m woody shrubs in the regeneration ability of the yew in transects (Bullock, 1996), randomly located to cover a Mediterranean environments. Studying the regenerative representative area of the stand (ca. 4 ha). At each meter traits of the yew in the Sierra Nevada (SE Spain), we of the tape the presence/absence and the identity of seek to determine: vegetation covering ground were recorded at two points, 1 m each perpendicular to the transect (n=100 1. The regeneration ability of this population by its sampling points per transect, 1000 points total). age structure. 2. The distribution of juvenile yews by microhabitats 2.3. Seedling sampling and the role of nurse woody shrubs in relation to herbivore damage. Seedling (individuals below 5 years old) abundance and spatial distribution was sampled noting age and herbivore damage for each individual. Seedling counts 2. Material and methods were made in 30 quadrats of 4 m2 in the following dif- ferent habitats in the study area: yew, areas under the 2.1. Natural history and study site canopy of adult yews; pine, areas under the canopy of adult Scots pines; open, areas bare of woody shrubs; Yew is a slow-growing evergreen tree, its longevity NFFS, areas below non-¯eshy-fruited shrubs; and FFS, reaching up to 1000 years. Although in central Europe areas below ¯eshy-fruited shrubs. For the microhabitats and the British Isles this species can form dense stands under shrubs, and due to the diculty of ®nding or woodlets, in southern Europe it grows in small stands homogeneous surfaces of 4 m2, we used sampling areas (Tittensor, 1980; Kelly, 1981; HernaÂ ndez and Clemente, of variable surface areas (corresponding to the basal 1994; Hulme, 1996, 1997). Yew is dioecious and wind- area of the shrub), covering a minimum of 30 sample pollinated. Every year, female individuals bear axillary units and 100 m2 (NFFS: n=83 sample units, 123 m2; cones which in autumn develop ¯eshy red arils containing FFS: n=35, 201 m2). Additionally, we considered as a a single seed. In the Mediterranean mountain areas, microhabitat the area surrounding a mountain spring seeds are dispersed mainly by frugivorous birds (Turdus (n=22 quadrats) located in the study site, in order to merula, T. torquatus and T. viscivorus; authors' personal control for the possible eects of higher water avail- observation). Dispersed seeds are strongly dormant but ability in yew recruitment, as shown for other woody do not form a persistent seed bank (Melzack and Watts, species in Mediterranean montane areas [see GarcõÂ aet 1982; Zhiri et al., 1994; Hulme, 1996). During this post- al. (1999) for J. communis]. dispersal stage, seeds can be predated by rodents [mainly the woodmouse Apodemus sylvaticus; see Hulme 2.4. Spatial distribution of saplings (1996, 1997)]. Seedlings start to emerge in the second spring after seedfall (Melzack and Watts, 1982). Yews Saplings (non-reproductive individuals 55 years old) can suer herbivory by insects and, especially severe, by spatial distribution and habitat was studied using two browsing ungulates which damage leaves, shoots and variables: (1) Angle of contact (), angle of direct con- bark (Tittensor, 1980; Kelly, 1981; Allison, 1990a,b). tact between the yew and the surrounding shrubs; and This study was conducted in 1998±1999 in an auto- (2) Shrub cover, percentage of soil surface covered by chthonous montane pine stand located near Trevenque woody vegetation in four 1-m transects in the cardinal peak (1700 to 1950 m a.s.l.; 37060N, 3210W; Sierra axis centered on the sapling and with sampling points at Nevada, Granada, SE Spain), composed of native Pinus 0.25, 0.5, 0.75 and 1 m from the yew. Depending on the sylvestris var. nevadensis, with a dense shrub understory. level of association with shrubs described by these vari- The climate is of Mediterranean mountain type, with ables, the habitat for each sapling was assigned to one rainfall (825 mm year1, average 1990±1998) heaviest in of three main categories: (a) open, when the yew grew in autumn and spring, hot dry summers and cold snowy a open site or was surrounded by <180 of woody winters. The area supports natural populations of Capra shrubs directly in contact with it; (b) NFFS, when the pyrenaica year round and extensive livestock during the yew was surrounded by 5180 of non-¯eshy-fruited summer [domestic goats and sheep; HoÂ dar et al., woody shrubs; and (c) FFS, when the yew was surrounded (1998)]. Furthermore, the forest is visited during by 5180 of ¯eshy-fruited woody shrubs. We did not con- autumn and winter by thrushes which actively feed on yew sider the habitats pine and yew in the case of saplings fruits [authors' personal observation; see also Jordano because very few saplings were found growing under these (1993)]. tree species, and all of them were simultaneously growing D. GarcõÂa et al. / Biological Conservation 95 (2000) 31±38 33 under ¯eshy-fruited shrubs (and, thus, were classi®ed rate diered between damaged and undamaged sap- under this category). In addition, we estimated the age lings, we used an ANCOVA, introducing damage as of the saplings as the number of whorls of the main independent variable, height as covariate and the rate of shoot [for this procedure with other conifers, see Ede- height growth as a dependent variable (Dowdy and nius et al. (1995); HoÂ dar et al. (1998)]. Wearden, 1991). Signi®cance of the statistical analyses was ®xed to the standard level, P<0.05 (Zar, 1996). 2.5. Herbivore damage on juvenile yews in relation to However, to avoid type-I error when statistically ana- protection by shrubs lysing more than one related variable, we chose the sequential Bonferroni test for ®tting the signi®cance The intensity of herbivory was quanti®ed for all juve- level (see Rice, 1989). nile yews (seedlings and saplings) by means of three parameters: (1) risk of herbivory, percentage of browsed plants; (2) damage intensity, proportion of shoots 3. Results damaged by ungulates, quanti®ed by counting the number of total shoots as well as the number of shoots 3.1. Habitat structure and spatial distribution of juvenile browsed by ungulates; and (3) magnitude of repeated yews herbivory (% losses). We considered the proportion of losses of apical dominance (that is, the number of apical The study plot was covered mainly by ¯eshy-fruited dominance losses divided by the age of the yew) as an shrubs, the dominant species being Juniperus communis, estimate of the herbivory pressure undergone by each J. sabina, Berberis hispanica and Rosa spp. (Table 1). juvenile since establishment [see HoÂ dar et al. (1998), for The density of seedlings varied signi®cantly between a similar procedure]. The association between the juve- habitats, with the areas under ¯eshy-fruited shrubs nile yews and the surrounding vegetation, in relation to showing the highest density values (Fig. 1; H=22.15, herbivory, was assessed by two complementary indexes: P=0.0005, df=5, Kruskall±Wallis test). The areas (1) shrub height (cm), maximum height of the shrub making direct contact with the yew; and (2) overgrowth (cm), dierence between the height of the yew and the Table 1 maximum height of the shrub in direct contact with the Habitat structure (percentages of cover of dierent plant species) in the study plota yew. A negative value of this variable indicates that the shrub overgrows the yew. In addition, the rate of height % cover growth of each tree was estimated by dividing its height by Pinus sylvestris 21.3 its age [see Danell et al. (1991) for a similar procedure]. Taxus baccata 3.0 Acer granatense 1.7 2.6. Yew population structure Lonicera arborea 2.0 Æ Trees 28.0 The following parameters were used to characterize Amelanchier ovalis 0.4 population structure: (1) population density (no. of Berberis hispanica 11.6 1 individuals ha ). This density is expressed using as raw Cotoneaster granatensis 0.3 data the total number of adults and saplings in a plot of Crataegus granatensis 0.4 1.9 ha located in the centre of the study area. The den- Juniperus communis 16.9 sity of seedlings was calculated by extrapolating to the Juniperus sabina 11.8 Prunus ramburii 3.5 entire plot, according to the coverage of the dierent Rosa spp. 4.6 habitats, the data collected in the sampling quadrats Other ¯eshy-fruited shrubs 1.0 (see Section 2.3); (2) age structure, expressed by the Æ Fleshy-fruited shrubs 50.5 percentages of adults, saplings and seedlings in the population; (3) sex ratio; and (4) ratio of seedling to Astragalus granatensis 0.1 adult density [see also Hulme (1996)]. Adult age was Erinacea anthyllis 3.9 estimated from trunk basal diameter assuming a mean Genista versicolor 6.4 Ononis aragonensis 10.5 1 annual growth rate of 1 mm year [see Hulme (1996) Salvia oxyodon 0.2 for a comprehensive description of this assumption]. Sex Other non-¯eshy-fruited shrubs 2.2 was determined by the presence of male or female cones. Æ Non-¯eshy-fruited shrubs 23.3

2.7. Statistical analysis Grasses 11.7 Bare ground 11.6 Rock 2.7 Most of the statistical analyses were performed using non-parametric statistics. To test whether the growth a n=100 sampling points per transect, 1000 points as a whole. 34 D. GarcõÂa et al. / Biological Conservation 95 (2000) 31±38 underyewcanopy,aswellasthoseclosetothemountain damage reaching 67.7% in some individuals. The mag- spring showed intermediate densities of seedlings, whereas nitude of repeated herbivory positively and signi®cantly under pine and non-¯eshy-fruited shrubs registered low correlated with damage intensity (=0.737, P<0.05 densities. No seedling was found in the open micro- after Bonferroni adjustment, n=101). In addition, the habitat (Fig. 1). percentage of losses of apical dominance was sig- Saplings were associated with ¯eshy-fruited shrubs ni®cantly higher in damaged plants than in undamaged more than expected according to shrub cover (see Table ones (19.12.3% vs. 3.41.5%, U=171.50, Z=7.35, 1) in the study plot ( 2=18.81, P<0.0001, df=2; Fig. 2). P<0.0001, Mann±Whitney test). Most juveniles (saplings+seedlings) were thickly sur- Undamaged seedlings and saplings were younger than rounded by woody shrubs, showing high values in the damaged ones (Table 2). In addition, damage intensity angle of contact and in the shrub cover in the sur- was positively and signi®cantly correlated with height rounding patch (Fig. 3). Very few yews overgrew the and age (>0.260, P<0.05 after Bonferroni adjust- nurse shrubs, most of these being 50 cm below the upper ment, n=86, for both Spearman rank correlations). border of the shrub (Fig. 3). The risk of being browsed signi®cantly declined with increased the angle of contact, the shrub cover and the 3.2. Herbivore damage in relation to shrub protection height of the nurse shrub above the yew (Table 2). Fur- thermore, damage intensity decreased signi®cantly with Ungulate herbivores attacked 31.1% of the 103 label- a greater angle of contact, the shrub cover and the led juvenile yews. Damaged plants lost an average of height of the nurse shrub (<0.260, P<0.05 after 23.03.6% (n=31) of their shoots to ungulates, Bonferroni adjustment, n=86). There was a positive

Fig. 1. Mean value (+1 S.E.) of the density of seedlings (no. of seedlings m2) found in dierent microhabitats in the study site (see Methods for microhabitat description).

Fig. 3. Distribution of values of the angle of contact with nurse shrubs, the percentage of contacts with woody shrub in the surround- Fig. 2. Comparison between the dierent habitats occupied by sapling ing path and the overgrowth distance with the shrub measured in the yews in the study plot and the availability of these habitats in the area, juvenile yews. Positive overgrowth values indicate that yew overgrows estimated as the cover according to Table 1. the shrub and negative values that the shrub overgrows the yew. D. GarcõÂa et al. / Biological Conservation 95 (2000) 31±38 35

Table 2 Mean values ( 1 S.E.) of the individual traits (Height and Age) as well as the characteristics related with the presence of surrounding nurse shrubs (Angle of contact, Shrub cover, Shrub height, Overgrowth) measured on juvenile yews, depending on ungulate herbivory (damaged vs undamaged)a

Damaged Undamaged 2 P

Height (cm) 53.475.91 (32) 38.915.96 (69) 2.16 0.141 Age (years) 15.971.85 (32) 9.271.19 (71) 8.49 0.0036 Angle of contact () 226.4127.42 (32) 301.9713.57 (71) 6.91 0.0086 Shrub cover 69.765.69 (31) 85.872.95 (69) 6.79 0.0091 Shrub height (cm) 81.5410.94 (26) 113.767.61 (64) 5.92 0.0153 Overgrowth (cm) 23.5810.29 (26) 72.598.37 (63) 11.88 0.0006

a The sample size for each group is shown in parentheses. The results of the logistic regression relating these variables with the probability of being damaged are also shown.

relationship between overgrowth and damage intensity Table 3 (=0.423, P<0.05 after Bonferroni adjustment, n=86). Summary of the ANCOVA analysis to compare the rate of height The more the juveniles were hidden beneath shrubs, the growth values (Height/Age) between damaged and undamaged yew juveniles lower was the intensity of damage (Table 2). Herbivory was associated with a signi®cant growth- df SS FP rate depression in juvenile yews (Table 3), with damaged Model 2 3.17 10.04 <0.0001 plants showing a lower rate of height growth Herbivory 1 1.12 7.11 0.0008 (3.630.30 cm/year) than undamaged ones (4.090.20 Height 1 2.47 15.69 <0.0001 cm/year). Error 98 15.46

3.3. Population structure

The estimated density of yews in the study plot was Table 4 1 287.9 individuals ha1, most individuals being seedlings, Density (no. of individuals ha ) and percentage of yews belonging to dierent stage-classes in the study plot and adults and saplings showing similar frequency of appearance (less than 10%; Table 4). The sex ratio was Density % strongly female biased, with 2.3 females per male Adults 22.63 7.86 (P=0.003, binomial test). Adult age ranged from 60 to Saplings 27.89 9.69 1050 years (Fig. 4), with males tending to be younger Seedlings 237.37 82.45 than females (Fig. 4), although there was no between- sex dierence in age (Z=0.916, P=0.359, median test). Most of saplings ranged between 10 and 30 years ture oered by our population may be due to the high and seedlings distributed around 3 years (Fig. 4). value of ¯eshy-fruited plant cover [>50% in our study site, higher than in other similar mountain localities in SE Spain; GarcõÂ a (1998)], the habitat where most of 4. Discussion seedlings and saplings appeared. Additionally, the reported dierences between our data and those of pre- Our yew population was characterized by an active vious surveys may be related to the speci®c methodol- regeneration under natural conditions. Considering the ogy and the habitat considerations we used to sample density and proportion of seedlings and saplings as an seedlings, which are dicult to detect in extensive sur- indicator of recruitment, our results are similar to or veys due to their small size and hidden location under even more favourable than those from other European shrubs. populations, outside the Mediterranean climate, where conservation status is favourable (see data from Hulme, 4.1. Seedling and sapling association to ¯eshy-fruited 1996). The conservation value of this population is shrubs reinforced when considering the current status of this species in southern Spain, where all the reported popu- Most yew seedlings were under ¯eshy-fruited shrubs, lations are composed of a few senescent adults and but also under adults and close to the mountain spring where regeneration appears to have collapsed, present- (Fig. 1). The association between ¯eshy-fruited plants ing a high risk of extinction (HernaÂ ndez and Clemente, and yew seedlings also applied to saplings which, how- 1994; Junta de AndalucõÂ a, 1998). The contrasting pic- ever, were absent from areas under adults and, especially, 36 D. GarcõÂa et al. / Biological Conservation 95 (2000) 31±38

Fig. 4. Box plots representing the age (in years) of adult (males and females), sapling and seedling yews in the population studied. from the water spring. This situation contrasts with Our results indicate that the protection of the yew by those found for other similar boreal-origin woody ¯eshy-fruited shrubs against herbivores is an additional species in Mediterranean mountains, where wet mea- factor determining the associative pattern between dows close to springs are the habitats most favourable juvenile yews and shrubs. Shrubs provide shelter against for the recruitment both of seedlings and of saplings ungulates both for their relative unpalatability and [GarcõÂ a et al. (1999) for J. communis]. Although our imbricate branching structure (in the case of shrubs study does not discriminate between seed input and such as J. communis and J. sabina, accounting for 29% seedling establishment, considering that ¯eshy-fruited of total coverage) or to dense spinescence (in the case of shrubs are the best habitats for seedling and sapling B. hispanica, Rosa spp. and Prunus ramburii, accounting establishment, our results suggest a clear spatial con- for 20% of total coverage). As a result, ungulates cordance throughout dierent phases of yew recruitment attacked almost exclusively plants unprotected by (see also Jordano and Herrera, 1995; Schupp and shrubs, juvenile yews suering serious damage, the main Fuentes, 1995). consequence of which is aggravated growth delay in a The origin of the association between yew and ¯eshy- slow-growing species [Callaway (1995); Zamora et al. fruited shrubs can be explained by two non-exclusive (1999); see also HoÂ dar et al. (1998) for a similar eect factors. Firstly, Mediterranean ¯eshy-fruited plants on P. sylvestris in Mediterranean mountains]. Thus, attract high numbers of avian frugivores during fall and spiny and unpalatable shrubs serve the purpose of fen- winter, acting as sinks where the seeds of many species, ces that are often used to exclude plants from herbivores the yew among them, accumulate disproportionately in conservation programmes. Finally, the mechanism of (Izhaki et al., 1991; Debussche and Isenmann, 1994; yew regeneration by shrub facilitation found in this Herrera et al., 1994; GarcõÂ a, 1998). This idea is reinforced study can be extrapolated to other populations with by the lack of establishment under non ¯eshy-fruited eective regeneration, even beyond the Mediterranean shrubs, places where the seed rain by avian frugivores environment, corroborating the fact that yew popula- rarely occurs. Secondly, the role of ¯eshy-fruited shrubs tions can establish after the development of shrublands as nurse plants is, primarly, related to the favourable in central Europe (Watt, 1926; Tittensor, 1980; Hulme, microenvironmental conditions for germination and 1996). ®rst-year seedling survival found under shrubs, com- pared to the situation in open areas. These conditions 4.2. Ecological consequences for conservation and are related mainly to soil moisture and the consequent restoration protective role against summer drought, soil texture and nutrient availability (Jore and Rambal, 1993; Callaway, The presence of yew in Andalusia is restricted mainly 1995; VerduÂ and GarcõÂ a-Fayos, 1996; GodõÂ nez-Alvarez to shady, foggy ravines in northward-facing montane and Valiente-Banuet, 1998). Once established, seedling- areas (Franco, 1986). However, the senescent status of to-sapling transition can be favoured under shrubs, due reported populations (HernaÂ ndez and Clemente, 1994; to the characteristic shade tolerance of the juvenile yews Junta de AndalucõÂ a, 1998) suggests that these environ- for growth (Tittensor, 1980; Hulme, 1996). Thus, the mental microclimatic conditions are necessary but not overall outcome of shrub±yew interaction appears to be sucient to ensure active regeneration of yew populations. facilitation in favour of, rather than competition This study suggests that patterns of yew regeneration are against, the yew. strongly dependent on the presence of ¯eshy-fruited D. GarcõÂa et al. / Biological Conservation 95 (2000) 31±38 37 shrublands. Considering a ®ne spatial scale, ¯eshy-fruited Danell, K., NiemelaÈ , P., Varvikko, T., Vuorisalo, T., 1991. Moose plants act as establishment microhabitats for yew seedlings browsing on Scots pine along a gradient of plant productivity. and saplings. From a macrohabitat scale, the presence Ecology 72, 1624±1633. Debussche, M., Isenmann, P., 1994. Bird-dispersed seed rain and of a well-developed community of ¯eshy-fruited shrubs seedling establishment in patchy Mediterranean vegetation. Oikos determines a site-dependent regeneration in yew popu- 69, 414±426. lations (see also Crawley and Long, 1995; Hulme, 1996). Dowdy, S., Wearden, S., 1991. Statistics for Research, 2nd Edition. This study exempli®es the presence of a complex Wiley Interscience, New York. facilitative system, composed of yews, ¯eshy-fruited Edenius, L., Danell, K., Nyquist, H., 1995. Eects of simulated moose browsing on growth, mortality, and fecundity in Scots pine: rela- nurse plants and avian dispersers. Yews bene®t from tions to plant productivity. Canadian Journal of Forest Research ¯eshy-fruited shrubs that can facilitate yew seed rain 25, 529±535. (indirect eect, mediated by avian dispersers) but also Font Quer, P., 1995. Plantas Medicinales: El DioscoÂ rides Renovado, protect against summer drought during the seedling 15th Edition. Labor, Barcelona. stage, and against ungulate herbivores during sapling- Franco, J.A., 1986. Taxus baccata L. In: Castroviejo, S., LaÂ nz, M., Â stage (direct eects). In view of these bene®ts, two main Lopez, G., Monserrat, P., MunÄ oz, F., Paiva, J., Villar, L. (Eds.), Flora Iberica, Vol. I: Lycopodiaceae±Papaveraceae. Real JardõÂn management guidelines can be suggested: (1) the main- BotaÂ nico, Servicio de Publicaciones del C.S.I.C, Madrid, pp. 201±202. tenance of healthy yew populations in Mediterranean GarcõÂ a, D., 1998. RegeneracioÂ n natural del enebro Juniperus communis mountains is strongly dependent on the conservation of L. en aÂ reas de alta montana mediterraÂ nea: conectando la ecologõÂ a well-developed ¯eshy-fruited shrublands and their com- reproductiva con el reclutamiento poblacional. PhD thesis, Uni- versidad de Granada, Granada. munity of avian dispersers; and (2) any restoration GarcõÂ a, D., Zamora, R., HoÂ dar, J.A., GoÂ mez, J.M., 1999. Age struc- planning for the yew in Mediterranean mountains ture of Juniperus communis L. in the Iberian peninsula: conservation should consider ¯eshy-fruited shrubs as the optimal sites of remnant populations in Mediterranean mountains. Biological for man-made planting of seedlings and saplings. Conservation 87, 215±220. GodõÂ nez-Alvarez, H., Valiente-Banuet, A., 1998. Germination and early seedling growth of Tehuacan Valley cacti species: the role of soils and seed ingestion by dispersers on seedling growth. Journal of Acknowledgements Arid Environments 39, 21±31. HernaÂ ndez, J.E., Clemente, M., 1994. ProteccioÂ n de la Flora en We thank the ConsejerõÂ a de Medio Ambiente, Junta AndalucõÂ a. Junta de AndalucõÂ a, ConsejerõÂ a de Cultura y Medio de AndalucõÂ a, for permitting our ®eld work in the Nat- Ambiente, Agencia de Medio Ambiente, Sevilla. Â ural Park of Sierra Nevada. The work has bene®ted Herrera, C.M., Jordano, P., Lopez-Soria, L., Amat, J.A., 1994. Recruitment of a mast-fruiting, bird-dispersed tree: bridging frugi- from the information and comments of two anonymous vore activity and seedling establishment. Ecological Monographs referees. David Nesbitt improved the English version. 64, 315±344. This study was supported by a grant PFPU-MEC and a HoÂ dar, J.A., Castro, J., GoÂ mez, J.M., GarcõÂ a, D., Zamora, R., 1998. postdoctoral fellowship from the University of Granada Eects of herbivory on growth and survival of seedlings and saplings of Pinus sylvestris nevadensis in SE Spain. In: Papanastasis, to D.G., a grant PFPI-MEC to J.C., and projects AMB95- V.P., Peters, D. 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