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Competitive effects of herbs on Quercus faginea seedlings inferred fromvulnerability curves and spatial-pattern analyses in a Mediterranean stand(Iberian System, northeast Spain)Author(s): Jordán Esteso-Martínez , J. Julio Camarero , Eustaquio Gil-PelegrínSource: Ecoscience, 13(3):378-387. 2006.Published By: Centre d'études nordiques, Université LavalDOI: http://dx.doi.org/10.2980/i1195-6860-13-3-378.1URL: http://www.bioone.org/doi/full/10.2980/i1195-6860-13-3-378.1

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13 (3): 378-xxx (2006)13 (3): 378-387 (2006)

Recent changes in land use and management of wood-lands in Mediterranean areas have resulted in new distur-bance regimes whose implications for the regeneration of these forests are still poorly understood. The changes

include abandonment of the traditional use of oak coppice stands, resulting in an increase in tree cover and density (Serrada, Allué & San Miguel, 1992). These land-use modi-fications may affect oak recruitment patterns, especially in Mediterranean woodlands where climatic stress constrains seedling survival (Bran et al., 1990; Bacilieri et al., 1993; Retana et al., 1999). Furthermore, several researchers have noted a lack of sexual regeneration by several oak species in

Competitive effects of herbs on Quercus faginea seedlings inferred from vulnerability curves and spatial-pattern analyses in a Mediterranean stand (Iberian System, northeast Spain)1

Jordán ESTESO-MARTÍNEZ, J. Julio CAMARERO2 & Eustaquio GIL-PELEGRÍN, �nidad de Recursos�nidad de Recursos Forestales, Centro de Investigación y Tecnología Agroalimentaria, Gobierno de Aragón, Apdo. 727, 50080 Zaragoza, Spain, e-mail: jjcamarero@aragon.es

Abstract: In recent years, several researchers have noted a lack of sexual regeneration by several oak species in Mediterranean coppice woodlands of the Iberian Peninsula. The abandonment of the traditional use of oak coppice stands has resulted in an increase in tree cover and density, which may affect microhabitat availability and oak recruitment. Microenvironmental heterogeneity is known to determine the successful recruitment of some Mediterranean oak species, but few studies have evaluated how competitive effects of herbaceous vegetation constrain oak recruitment at small spatial scales. We indirectly assessed how the herbaceous understory interacts with Quercus faginea recruitment in a stand in northeast Spain by (1) establishing the vulnerability of seedling xylem to cavitation as related to the water potential in healthy seedlings located outside herb patches and unhealthy seedlings situated within these patches and (2) characterizing the small-scale spatial pattern of Q. faginea regeneration and herb cover as related to other environmental factors. We mapped all individuals located within a 20- × 20-m plot, which was subdivided into 400 quadrats of 1 m2 each, to estimate litter depth, herb and shrub cover, and sunlight in the understory. Water potentials of Q. faginea individuals decreased in the following order: adults > sprouts > healthy seedlings > unhealthy seedlings. The summer soil-water content in the uppermost 40 cm of the soil was lower in microsites within dense herb patches than in those with low herb cover. Dense herb cover was positively associated with a greater density of unhealthy Q. faginea seedlings. Our results indicate that competition with the understory herbs for soil water should be regarded as one of the main factors controlling recruitment of Mediterranean oaks.Keywords: Brachypodium, Crataegus monogyna, Quercus, recruitment, water potential.

Résumé : Plusieurs chercheurs ont remarqué récemment une absence de régénération sexuelle chez plusieurs espèces de chênes des taillis méditerranéens de la péninsule Ibérique. L’abandon de l’utilisation traditionnelle des taillis de chênes a causé une augmentation du couvert et de la densité des arbres, ce qui peut affecter la disponibilité des micro-habitats et le recrutement de chênes. Bien que l’on sache que l’hétérogénéité micro-environnementale détermine le succès de recrutement de certaines espèces méditerranéennes de chênes, peu d’études ont évalué l’effet compétitif de la végétation herbacée en tant que contrainte au recrutement du chêne à petite échelle spatiale. Nous avons déterminé indirectement comment le sous-étage herbacé interagit avec le recrutement de Quercus faginea dans un peuplement du nord-est de l’Espagne : (i) en déterminant la vulnérabilité du xylème des graines à la cavitation en relation avec le potentiel hydrique de graines en santé situées à l’extérieur de parcelles d’herbes et de graines malades situées à l’intérieur de ces parcelles et (ii) en caractérisant le patron de distribution spatiale de la régénération de Q. faginea et du couvert herbacé en relation avec d’autres facteurs environnementaux. Nous avons cartographié tous les individus dans une parcelle de 20 × 20 m qui a été subdivisée en 400 quadrats de 1 m2 chacun pour mesurer l’épaisseur de la litière, le couvert herbacé et arbustif et la luminosité en sous-étage. Les potentiels hydriques des individus de Q. faginea diminuaient dans l’ordre suivant : adultes > rejets de taillis > graines en santé > graines malades. Le contenu estival en eau dans les premiers 40 cm de sol était moins élevé dans les microsites situés à l’intérieur de parcelles ayant une forte densité d’herbes que dans celles ayant un faible couvert herbacé. La densité d’herbes était associée positivement à une plus grande densité de graines malades de Q. faginea. Nos résultats indiquent que la compétition pour l’eau du sol avec les herbacées en sous-étage devrait être considérée comme l’un des facteurs principaux contrôlant le recrutement des chênes méditerranéens.Mots-clés : Brachypodium, Crataegus monogyna, potentiel hydrique, Quercus, recrutement.

Nomenclature: Castroviejo et al., 1986.

Introduction

1Rec. 2005-06-06; acc. 2006-01-17. Associate Editor: Christian Messier.2Author for correspondence.

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Mediterranean woodlands of the Iberian Peninsula (Pulido, Díaz & Hidalgo de Trucios, 2001). These authors have sug-gested several explanations for the low recruitment rates, ranging from a lack of suitable regeneration microsites caused by the new disturbance regime to increasing climatic stress caused by global warming.

The negative effect of climatic stress on oak recruit-ment in Mediterranean woodlands is usually exacerbated by indirect competition with the understory herbaceous vegeta-tion (Gordon & Rice, 2000). Nevertheless, the competitive effects of herbaceous vegetation on oak recruitment pat-terns at small spatial scales have not been assessed, despite the fact that microenvironmental heterogeneity is known to determine successful recruitment of Mediterranean oak species (Gómez, 2004). Seedlings and sprouts represent the main modes of oak regeneration, which varies accord-ing to the disturbance regime (Larsen & Johnson, 1998; Espelta, Sabaté & Retana, 1999). However, the functional thresholds for recruit survival (e.g., water potential) have not been established for the two types of regeneration as related to their location in different microsites. For instance, the vulnerability of xylem to cavitation and the desiccation tolerance of recruits may differ between conspecific oak seedlings and sprouts, and between seedlings situated within and outside dense herb patches.

In this study, we assess how herb cover and environ-mental conditions limit the recruitment of a Mediterranean oak species (Quercus faginea) at small spatial scales. We expect higher mortality of Q. faginea seedlings in sites where the herb cover is dense due to the competition between seedlings and herbs. In addition to negative interac-tions, positive interactions greatly affect oak recruitment in Mediterranean woodlands (Rousset & Lepart, 1999; 2000). Thus, a significant spatial association between Q. faginea seedlings and nurse plants such as shrubs might also sug-gest direct or indirect facilitative effects on oak recruitment. To identify the mechanisms controlling the establishment of Q. faginea, we focus on two objectives: (1) to character-ize the xylem water potential of seedlings located within and outside dense herb patches as related to the vulner-ability of xylem to cavitation and (2) to describe the pattern of Q. faginea regeneration at a small spatial scale and its controlling abiotic (e.g., light) and biotic factors (e.g., herb cover). The fulfillment of these aims will provide a deeper understanding of how the understory affects Q. faginea recruitment in different microhabitats.

MethodsStudy SItE

We established a 20- × 20-m plot within a topographi-cally homogeneous site in a coppice stand in the Iberian System, northeast Spain (41° 05' N, 1° 25' w, 800 m asl). We used recruitment data from this single plot instead of using data from smaller replicated subplots because the mean den-sity of oak seedlings from five 5- × 5-m subplots randomly located within the study plot did not differ significantly (P > 0.05, Kruskall–Wallis test). According to data from a nearby meteorological station (Daroca, 41° 07' N, 1° 25' w, 779 m, 1965–2002 data), the climate at the study site is

Mediterranean with continental influence. The mean annual temperature is 12.6 °C, and the total annual precipitation is 420 mm. The drought period lasts from July to September. The soils are calcareous sandy loams that developed on limestone. The study area was previously dominated by coppice stands of Quercus ilex and Q. faginea. Traditional coppice management in this area ceased in the 1960s. In 1978, most of the area was reforested with Pinus halepen-sis; however, a mixed coppice stand remained on the study site. In 1989, a selective thinning was carried out at the study site. Currently, Q. faginea is the most abundant tree found on the site.

FIEld SamplINg As we were interested in the local heterogeneity of

environmental factors affecting oak regeneration at small spatial scales, the plot was subdivided into quadrats (1 m2, n = 400) to describe the microenvironmental conditions affecting Quercus regeneration within each quadrat. The southwest corner of each quadrat was mapped and perma-nently tagged. All trees and shrubs were mapped with an accuracy of 0.01 m using a Leica TCA2003 total station (Leica Geosystems, Heerbrugg, Switzerland) and then converting distances and angles from a reference starting point to coordinates in a Cartesian plane (x, y). In the case of multistemmed individuals, the stem with the largest basal diameter was regarded as the central position of the individual. In addition to trees, we also mapped the stumps of Q. faginea and Q. ilex, which were classified accord-ing to their type of wood (Q. faginea = ring-porous wood; Q. ilex = diffuse-porous wood). Stumps were regarded as trees logged in 1989.

To estimate soil water availability across a vertical profile, a 2-m-deep pit was excavated in the middle of the plot. Vertical changes in the gravimetric soil water content (%) were estimated by taking two 33-cm3 soil samples every 0.5 m along the soil profile during an exceptionally dry day in August 2001. To estimate soil water availability in two contrasting microsites (within and outside dense herb patches), changes in the gravimetric soil water content (%) were estimated by taking 33-cm3 soil samples in the upper 20 and 40 cm of the soil during the same dry day in August 2001. We took soil samples randomly located within the study plot but situated at least 5 m apart, since the mean size of herb-cover patches was 5 m. We took 10 soil samples for each depth at each of the two contrasting microsites.

The substrate and plant cover were classified into three vertical strata: (1) the basal stratum (height < 20 cm), which included substrate (soil, litter), herbs (mainly Brachypodium phoenicoides and Festuca rubra), stumps (mainly Q. ilex), Crataegus monogyna seedlings, Q. faginea seedlings, and sprouts (Q. faginea, Q. ilex); (2) the intermediate stratum (height = 0.2–4.0 m), including adult shrubs (C. monogyna, Lonicera xylosteum, Rosa spp., Rubus spp.) and unma-tured Q. faginea young individuals (height = 1.5-4.0 m); and (3) the top stratum (height > 4 m), dominated by adult Q. faginea and Q. ilex trees. Substrate (soil, litter, herb) and plant cover (%) for the two first strata were estimated visu-ally for each 1-m2 quadrat. In addition, litter depth was esti-mated using a semiquantitative scale: shallow (1, 0–5 cm),

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intermediate (2, 5–10 cm), and deep (3, > 10 cm). Those individuals whose height was lower than or equal to 0.2 m were considered seedlings. Seedlings and sprouts were dis-tinguished in the field using two characteristic traits: (1) the presence of cotyledonary leaves or attached residues of the acorn in the former and (2) the more vigorous early growth and the presence of rhizomes in the latter. Quercus faginea regeneration was also classified, according to its vigour, into healthy (1–50% dead leaves) and unhealthy (> 75% severely damaged or dead leaves) seedlings and sprouts. The vigour of most Q. faginea regeneration remained constant through time during 2001–2003. Thus, defoliation degree mainly reflected loss of hydraulic capacity caused by embolism, and, in a few cases, the effects of herbivores. In most cases, soil recharge during the wetter winter months did not lead to repair of the physical damage. We measured the size (dbh, diameter at breast height; height) of all stems taller than 1.3 m to estimate the basal area and size of the main woody species. A detailed description of variables measured in the stand is presented in Tables I and II.

To estimate the percent of full sunlight that would be likely to reach the understory of each quadrat, we took hemispherical photographs of the overstory. We estimated the integrated total transmitted radiation (mols·m-2·d-1) as an approximation of the percent of available sunlight trans-mitted to seedlings. Photographs were taken in the centre of the quadrats during the foliage-on period under completely overcast days. A Nikon Coolpix 990 digital camera (Nikon Corp., Tokyo, Japan) with a 180° hemispherical fisheye lens (Nikon fisheye converter FC-E8, equivalent to an 8-mm lens) was mounted on a tripod, levelled at 0.02 m above the ground, and oriented so that the top of the photographs always pointed north. The photographs were converted into black and white bitmaps, and they were analysed using the software Gap Light Analyzer 2.0 (Frazer, Canham & Lertzman, 1999). The threshold level for each image was subjectively selected within a narrow range. The study site

was not deeply shaded, which justified the use of hemi-spherical photographs.

We were more interested in post-summer than pre-sum-mer mortality because summer drought was expected to be the most limiting factor for oak recruitment. The annual survival rates of Q. faginea seedlings and sprouts locat-ed within the stand were estimated by monitoring tallied Q. faginea seedlings and sprouts monthly during the period 2001–2003.

vulNErabIlIty OF xylEm tO CavItatION

We studied xylem cavitation in order to establish a quantitative threshold for the survival and establishment of Q. faginea regeneration. To quantify the xylem vulner-ability to embolism we constructed a vulnerability curve for Q. faginea using shoots from 1-y-old seedlings grown under controlled conditions because these seedlings showed similar size and vigour. Seeds were collected from trees located in the experimental stand. Seedlings were grown in a greenhouse under uniform nutrient supply and light condi-tions without water restrictions. The mean temperature dur-ing the growing season (March–August) was 20 °C, and the relative air humidity ranged from 60 to 90%. A modification of the air injection developed by Jarbeau, Ewers, and Davis (1995) was used to establish the vulnerability curves. The vulnerability curve was fitted using a sigmoidal function (Pammenter & Vander Willigen, 1998):

[1]

where PLC is the percentage loss of hydraulic conductivity (kg·m·s-1 MPa-1), a is a constant describing the range of potentials over which conductivity decreases, Ψ is the water potential (MPa), and b is the water potential corresponding to a 50% loss of conductivity. The curve was fitted by least squares regression. Care must be taken when comparing xylem water potentials measured in the field with threshold values for cavitation measured in seedlings grown under

tablE I. Characteristics of variables measured in the study plot. Va-lues are means ± SE, except for basal area. Different letters indicate significant differences (P < 0.05; Mann–Whitney test).

Variable (units) Mean ± SESoil water content, S.W.C. (%), 4.79 ± 0.21a / 3.54 ± 0.24a0.5- / 1.0- / 1.5- / 2.0-m depth / 8.33 ± 0.26b / 10.76 ± 0.04bS.W.C. (%) inside / outside herb 6.29 ± 0.22a / 7.58 ± 0.47bpatches, 0.2-m depth (%)S.W.C. (%) inside / outside herb 5.98 ± 0.38a / 7.11 ± 0.48bpatches, 0.4-m depth (%)Transmitted radiation (mols·m-2·d-1) 6.19 ± 0.09Litter depth1 1.65 ± 0.03Herb cover (%) 23.37 ± 1.05Litter cover (%) 73.28 ± 1.08C. monogyna cover (%) 6.81 ± 0.66Q. faginea basal area (m2·ha-1) 21.91Q. ilex basal area (m2·ha-1) 5.58C. monogyna basal area (mm2·ha-1) 0.251Semiquantitative variable with three classes: shallow (1), intermediate (2),

and deep (3).

tablE II. Density and size (dbh, diameter at breast height; and hei-ght) of tree and shrub classes at the study plot. The size was measu-red only for stems taller than 1.3 m. Abbreviations starting with Qf, Qi, and Cm are for Q. faginea, Q. ilex, and C. monogyna, respecti-vely. The remaining characters indicate size or regeneration class: a, adults; y, young individuals; s, seedlings; r, sprouts; st, stumps. The vigour classes for recruitment are healthy and unhealthy seedlings and sprouts. Values are means ± SE.

Species and life-stage Density (stems·ha-1) Dbh (cm) Height (m)Qf a 1100 14.8 ± 0.7 8.3 ± 0.3Qf y 1875 1.3 ± 0.1 2.6 ± 0.1Qf s healthy 13,075 Qf s unhealthy 2800 Qf r healthy 11,550 Qf r unhealthy 1550 Qf st 350 Qi a 300 11.6 ± 0.7 6.3 ± 0.3Qi s 0 Qi r 18,100 Qi st 650 Cm a 1800 1.0 ± 0.1 2.8 ± 0.1Cm s 7850

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different environmental conditions because this comparison is a rough approximation.

xylEm watEr pOtENtIal

The water status of oak seedlings may reflect soil water potentials, which directly influence seedlings’ growth and survival. To assess the plant water status during summer, predawn and midday xylem water potentials were measured in the field during the same day as the soil water content. Measurements were performed using a Scholander pressure chamber. They were carried out on leaf-covered twigs of Q. faginea adults, sprouts, and seedlings (five individuals per class, one twig per individual). In the case of the seed-lings, we considered separately healthy and unhealthy indi-viduals taken from outside and within dense herb patches, respectively. We followed the methodology of Ritchie and Hinckley (1975).

StatIStICal mEthOdS

Point Pattern analyses: K (d)-function

To describe the spatial pattern of stems we used point pattern analysis based on Ripley’s K (d), a second-order density function that considers the distances between all pairs of points (Ripley, 1977). We analyzed the spatial pattern of a class of points (univariate) and the interaction between two types of points (bivariate). Homogeneity and isotropy were assumed, but in the case of suspected het-erogeneity, the data were analyzed following Pélissier and Goreaud (2001). In a Poisson process the probability of occurrence of one point at any location is independent of the location of the other points. Thus, the Poisson process is used as a null hypothesis corresponding to Complete Spatial Randomness (CSR). Besag (1977) proposed replacing K (d) by L (d), where L (d) = (K (d) /π)0.5. This function stabi-lizes the variance of K (d) and is easier to interpret because L (d) – d = 0 under CSR. Aggregated and regular patterns will produce values of L (d) – d higher and lower than zero, respectively. We selected d = 0.5 m because this scale was appropriate for characterizing the small-scale spatial pat-terns of oak regeneration and their microenvironmental con-ditions. To estimate maximum aggregation, we calculated the W (d) index following Szwagrzyk (1990). If W (d) > 1 the pattern is clumped, if –1 < W (d) < 1 the pattern corre-sponds to CSR, and if W (d) < –1 the pattern is regular.

In the case of bivariate point patterns, the interactions between types of points (size, vigour, or regeneration class-es) were studied using K12 (d) and L12 (d) (Haase, 1995). If the two sets of points are independent, L12 (d) – d = 0. If the interaction is attractive or repulsive, L12 (d) – d > 0 and L12 (d) – d < 0, respectively. In all analyses, we used classes of individuals with n ≥ 25. Finally, we used the Monte Carlo method to generate 95% confidence intervals (10,000 simu-lations). For each random simulation, the values of the esti-mators were computed at each distance d, and the computed values were compared with those obtained with the real pattern. If the observed function for a distance d falls above or below the confidence bounds, the spatial structure is significantly (a = 0.01) aggregated or regular, respectively. In the bivariate analyses, the locations of the second set of points were randomized while keeping fixed the locations

of the first set of points. Spatial analyses were done using the ADE-4 package (Thioulouse et al., 1997).

sPatially corrected correlation

To determine the relationships between the main inde-pendent variables and regeneration, we used Pearson’s product-moment correlation coefficient (r). However, to evaluate the significance of correlation coefficients a cor-rection must be made to take into account spatial autocorre-lation (Clifford, Richardson & Hémon, 1989). For instance, if positive spatial autocorrelation exists, the effective sample size (m) will be less than the actual sample size (n), being a function of the degree of spatial autocorrelation (Dutilleul, 1993). Hence, the conventional probability level of the correlation (pConv) must be transformed into a corrected probability level (pCorr). For each 1-m2 quadrat, we used as independent variables the following: herb cover (%), sun-light (radiation in mols·m-2·d-1), litter depth (three classes), and C. monogyna cover (%). The cover of litter (%) was used instead of litter depth because the former is a quantita-tive variable and both are positively related. The rest of the cover data were discarded because of their low cover values (1–5%). The dependent variables were density of healthy and unhealthy Q. faginea sprouts and seedlings, obtained by converting point coordinates (x, y) into gridded density data for the 1-m2 quadrats. Finally, we estimated the mean patch size of herb cover and light availability using Moran’s I cor-relograms (Legendre & Fortin, 1989). The point at which the value of the autocorrelation coefficient crosses the abscissa in a correlogram provides an estimate of the mean size of the zone of influence of the variable (patch). These analyses were done using PASSAGE (Rosenberg, 2002).

ResultsQuercus faginea rECruItmENt aNd vulNErabIlIty OF xylEm tO CavItatION

The soil water content decreased significantly below the uppermost 1 m of the pit (Table I). The mean water content in shallow soil samples was significantly lower within dense herb patches than outside them (P < 0.05; Mann–Whitney test; Table I). During the 2001–2003 period, the mean annual survival rate (± SE) was slightly higher for Q. faginea sprouts (0.85 ± 0.04 y-1) than for conspecific seedlings (0.79 ± 0.06 y-1), but the two rates were not sig-nificantly different. The vulnerability curve of Q. faginea indicated that a 50% loss of conductivity was reached at a water potential circa –3.9 MPa (Figure 1). Predawn and midday water potentials of Q. faginea individuals decreased in the following order: adults > sprouts > healthy seedlings > unhealthy seedlings (Figure 2). Only unhealthy Q. faginea seedlings located within dense herb patches reached mid-day potentials significantly lower than the threshold of 50% loss of conductivity (P = 0.02, one sample t-test), but these potentials did not significantly differ from the threshold for 75% loss of conductivity (P = 0.42). Both predawn and midday potentials differed significantly (P ≤ 0.05) between all types of Q. faginea individuals.

SpatIal aNalySES

The spatial pattern of Q. faginea individuals showed an increasing degree of clumping as their size decreased

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(Table III). Adults showed CSR at all analyzed distances, young immature individuals showed aggregation at medium distances (0.5–5.5 m), and seedlings and sprouts showed aggregation at all distances. A similar result was found for C. monogyna adults and seedlings, with a distance of maxi-mum aggregation for C. monogyna seedlings of 2.0 m. The spatial pattern of Q. ilex sprouts showed significant aggrega-tion at all analyzed distances, with the most intense clumping at 1.5 and 6.0 m, this last value being close to the distance of maximum aggregation for the stumps (5.5 m). Both healthy Q. faginea seedlings and sprouts showed maximum aggrega-tion at 2.5 m. However, unhealthy Q. faginea seedlings and sprouts showed the most intense clumping at 4–5 m.

The spatial interactions of Q. faginea adults with healthy or unhealthy Q. faginea seedlings or sprouts did

not differ significantly from CSR for all distances. A similar result was obtained for Q. faginea young individuals and conspecific seedlings and sprouts. Healthy and unhealthy Q. faginea sprouts showed no significant spatial interac-tion, whereas the same vigour classes of seedlings did show spatial attraction at 0.5–3.0 m (Table IV). Stumps and Q. faginea sprouts did not show any significant departure from CSR, but we detected a significant spatial association between stumps and Q. ilex sprouts at 0.5-1.5 m (Table IV). Crataegus monogyna adults and healthy Q. faginea seed-lings showed spatial attraction at 1 m, while C. monogyna adults and seedlings were spatially associated at longer dis-tances. Nevertheless, the bivariate analysis between spiny shrubs (Rosa spp., Rubus spp.) and healthy Q. faginea seed-lings did not reveal any spatial interaction.

The strongest positive association of all types of oak regeneration with herb cover was observed for unhealthy Q. faginea seedlings (Table V, Figure 3). Litter cover was negatively related to the density of unhealthy Q. faginea seedlings. We detected a significant positive association between the cover of C. monogyna adults and the density of healthy Q. faginea seedlings. Light availability was not significantly related to seedling and sprout vigour (Table V, Figure 4). The negative relationship between light availabil-ity and the density of healthy Q. faginea seedlings was not significant due to the presence of positive spatial autocor-relation in both variables, which showed similar patch sizes. According to globally significant Moran’s I correlograms (P ≤ 0.05), herb cover and light availability showed signifi-cant positive spatial autocorrelation up to 5 and 3 m (mean patch sizes), respectively (results not presented).

DiscussionSeedling establishment is one of the main constraints

of tree recruitment in Mediterranean woodlands where com-petition with the understory vegetation may have a strong negative influence on seedling survival. In this study, water potential reached the lowest values for unhealthy Q. faginea seedlings located within dense herb patches, which suggests that competition with herbs for soil water may be among the main factors controlling Q. faginea recruitment. In addi-tion, we found during a typical dry summer day that the water content in the uppermost 40 cm of the soil was lower inside than outside dense herb patches, which suggests that soil water availability may differ between these two con-trasting microsites. The different soil water contents found for these microhabitats agree with the contrasting water potentials measured for unhealthy and healthy oak seedlings located within and outside the herb patches, respectively. Furthermore, the low water retention capacity of the sandy loam found at the study site may explain why the significant-ly different water potentials of unhealthy and healthy seed-lings result from moderate differences in soil water content.

The loss of xylem conductivity is the most likely cause of Q. faginea seedling mortality at the study site. �nhealthy oak seedlings showed values close to 75% loss of conduc-tance, which are similar to those reported by Tyree et al. (2003) for nearly dead seedlings of tropical woody species. Given that the vulnerability curve was based on seedlings grown under controlled and uniform environmental condi-

FIgurE 1. Vulnerability curve of Q. faginea considering the per-centage loss of conductivity (PLC) for different water potentials (Ψ). The lines indicate the water potential (–3.9 MPa) at which PLC = 50. The fit for individual values (empty circles) was highly significant (PLC = 100 / (1 + e1.21 (Ψ + 3.89)), R2 = 0.76, P ≤ 0.001). Error bars are stan-dard errors (SE).

FIgurE 2. Water potential at predawn and midday of Q. faginea individ-uals during a dry day in August 2001 according to their life stage and health status (adults, sprouts, healthy and unhealthy seedlings). Different letters correspond to significant differences (P ≤ 0.05) between types of individu-als according to two sample t-tests. Dotted and slashed lines correspond to 50% and 75% loss of conductance, respectively (see Figure 1).

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tions, we may have overestimated the percentage loss of conductivity for a given xylem water potential as compared with seedlings growing in the field if most of the latter did not present native embolism. For instance, the vulnerabil-ity to cavitation in Fagus sylvatica may acclimate to dif-ferent light conditions that might correspond to contrasting evaporative demands (Cochard, Lemoine & Dreyer, 1999). Nevertheless, our results provide a first estimate of the functional thresholds for recruit survival based on the vul-nerability of xylem to cavitation.

Our results also point to the relevance of direct com-petition between oak seedlings and herbs for successful recruitment, because herb cover was the factor most directly correlated to the density of unhealthy Q. faginea seed-lings. The competitive effects of grassland annuals on oak

seedlings include a reduction in light, soil water availabil-ity, and soil nitrogen concentration (Gordon & Rice, 2000). We suggest that Q. faginea recruitment and herb presence may be favoured in microsites with moderate water avail-ability in the shallow soil, but that subsequent competition between seedlings and herbs may lead to the presence of most unhealthy oak seedlings within dense herb patches. The spatial association between herb cover and unhealthy Q. faginea seedlings may explain the greater mortality rate for those seedlings located in areas within dense herb patch-es, as has been confirmed by manipulation experiments (Rey Benayas, Espigares & Castro-Díez, 2003). The exten-sive belowground rhizome of Mediterranean Brachypodium species allows them to access soil water to depths up to 50 cm, which may lead to a severe reduction of soil mois-ture and reduce the recruitment of woody species (Caturla et al., 2000). For instance, seeds of P. halepensis germinated poorly in sites dominated by Brachypodium species (Loisel, 1966). Moreover, competition for soil nutrients between B. phoenicoides and oak seedlings might also affect Q. faginea recruitment. In intensively managed Mediterranean sites such as the present study site, phosphorous losses in the upper 50 cm of the soil were considerable up to 40 y after the management ceased (Ruecker et al., 1998). In summary, B. phoenicoides and oak seedlings may compete for soil resources (water, nutrients), specifically in the uppermost levels of the soil where most of the belowground rhizome is found and where soil water content is lower than below.

The spatial scale of aggregation of unhealthy Q. faginea seedlings (5 m) roughly corresponded to the mean size of dense herbaceous patches. Although adults and sprouts

tablE III. �nivariate point patterns according to Ripley’s K (d) for different sets of stages and species. Abbreviations for species and life-stages are the same as in Table II. Abbreviations for symbols are: dots; random distribution and + are significant aggregated distribution. The class “shrubs” includes only spiny shrubs (Rosa spp., Rubus spp.). For each group of points, bold symbols indicate distances (d) with maximum aggregation (W (d) > 1).

d (m) 0.5 1 1.5 2 2.5 3 3.5 4 4.5 5 5.5 6 6.5 7 7.5 8 8.5 9 9.5 10Qf a · · · · · · · · · · · · · · · · · · · ·· · · · · · · · · · · · · · · · · · · · · · · · · · · · · · · · · · · · · · ·· · · · · · · · · · · · · · · · · · · · · · · · · · · · · · · · · · · · ·· · · · · · · · · · · · · · · · · · · · · · · · · · · · · · · · · · ·· · · · · · · · · · · · · · · · · · · · · · · · · · · · · · · · ·· · · · · · · · · · · · · · · · · · · · · · · · · · · · · · ·· · · · · · · · · · · · · · · · · · · · · · · · · · · · ·· · · · · · · · · · · · · · · · · · · · · · · · · · ·· · · · · · · · · · · · · · · · · · · · · · · · ·· · · · · · · · · · · · · · · · · · · · · · ·· · · · · · · · · · · · · · · · · · · · ·· · · · · · · · · · · · · · · · · · ·· · · · · · · · · · · · · · · · ·· · · · · · · · · · · · · · ·· · · · · · · · · · · · ·· · · · · · · · ·· · · · · · ·· · · · ·· · ··Qf y + + + + + + + + + + + · · · · · · · · ·· · · · · · · · · · · · · · · · ·· · · · · · · · · · · · · · ·· · · · · · · · · · · · ·· · · · · · · · · · ·· · · · · · · · ·· · · · · · ·· · · · ·· · ··Qf s healthy + + + + + + + + + + + + + + + + + + + +Qf s unhealthy + + + + + + + + + + + + + + + + + + + +Qf r healthy + + + + + + + + + + + + + + + + + + + +Qf r unhealthy + + + + + + + + + + + + + + + + + + + +Qi r + + + + + + + + + + + + + + + + + + + +Stumps + + + + + + + + + + + + + + + + + + + +Cm a + + + + + + + + · · · · · · · · · · · ·· · · · · · · · · · · · · · · · · · · · · · ·· · · · · · · · · · · · · · · · · · · · ·· · · · · · · · · · · · · · · · · · ·· · · · · · · · · · · · · · · · ·· · · · · · · · · · · · · · ·· · · · · · · · · · · · ·· · · · · · · · · · ·· · · · · · · · ·· · · · · · ·· · · · ·· · ··Cm s + + + + + + + + + + + + + + + + + + + +Shrubs + + + + + + + · · · · · · · · · · · · ·

tablE Iv. Bivariate point patterns according to Ripley’s K12 (d) between different sets of stages and species. Abbreviations for species, life-stages, and symbols are the same as in Tables II and III. Only spatial interactions showing significant departures from complete spatial randomness at any distance (d) are displayed.

d (m) 0.5 1 1.5 2 2.5 3 3.5 4 4.5 5 5.5 6 6.5 7 7.5 8 8.5 9 9.5 10Qf s healthy– Qf s unhealthy + + + + + + · · · · · · · · · · · · · ·Stumps–Qi r + + + · · · · · · · · · · · · · · · · · Cm a–Qf s healthy · + · · · · · · · · · · · · · · · · · · Cm a–Cm s · · · · · · · · · · + + + + · · · · · ·

tablE v. Spatially corrected correlation analyses. If spatial autocor-relation exists, the effective sample size (m) differs from the actual sample size (n), and the conventional probability level of the cor-relation (PConv) must be corrected (PCorr). Only correlations with PConv ≤ 0.05 are shown. The last column indicates loss (–) of signifi-cance after the correction. Abbreviations as in Tables I and II.

Variables r PConv PCorr m –Herb–Qf r 0.1720 0.0006 0.0628 118 –Herb–Qf s healthy 0.2002 0.0001 0.0379 108 Herb–Qf s unhealthy 0.3897 0.0001 0.0001 189 Light–Qf s healthy -0.1428 0.0042 0.4993 25 –Herb–Litter cover -0.9445 0.0001 0.0001 55 –Litter cover–Qf r -0.1184 0.0178 0.1812 129 –Litter cover–Qf s healthy -0.1392 0.0053 0.1301 120 –Litter cover–Qf s unhealthy -0.3648 0.0001 0.0001 201 Cm a–Qf s healthy 0.1893 0.0001 0.0056 212

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may access water from relatively deep in the soil profile, Q. faginea seedlings are probably unable to access deep sources of soil water (Weltzin & McPherson, 1997). Oak recruitment in mediterranean California woodlands was significantly inhibited when seedlings grew near annual herbs; there, soil water was rapidly depleted, leading to a drastic reduction of seedling growth (Gordon & Rice, 1993). Herbs may compete directly with oak seedlings for resources or act in combination with the litter layer (Facelli & Pickett, 1991) as a physical barrier blocking the access of the seedling radicle to the mineral soil (Borchert et al., 1989). In our case, litter depth was not related to the mortal-ity of Q. faginea seedlings, despite the fact that litter cover was associated with a low density of unhealthy Q. faginea seedlings because shaded microsites were characterized by high litter cover and low herb cover. However, the forest canopy was quite open at the study site, and the herb cover was dense both in sunny microhabitats and under Q. faginea adult trees (Figure 3). These findings do not prove the absence of indirect effects of litter cover on the perfor-mance of Q. faginea seedlings. For instance, Kostel-Hughes, Young, and Carreiro (1998) found that the seedlings of some oak species with large seeds, such as Q. rubra and Q. alba, performed better with a thick cover of leaf litter.

The point-pattern analyses did not reveal any spatial interaction between Q. faginea adult trees and seedlings,

despite the fact that a certain amount of competition for soil water might be expected between adult oaks and seedlings (Holmes & Rice, 1996). The first established trees may indi-rectly favour conspecific seedlings by increasing soil fertil-ity and by reducing light levels (Belsky, 1994; Li & Wilson, 1998). The non-significant negative relationship between light level and the density of healthy Q. faginea seedlings was due to the presence of positive spatial autocorrelation in both variables (Table III, Figure 4). The spatial scale of the mean patch size of light availability (3 m) was similar to the scale of maximum aggregation of healthy Q. faginea seed-lings (2.5 m). There might be an indirect facilitation of adult trees on oak seedlings if adult trees induce a reduction of transmitted radiation that decreases the competitive effect of grasses on oak seedlings (Pagès & Michalet, 2003; Siemann & Rogers, 2003). This indirect facilitation was probably not significant at the study site since the forest canopy was not very closed. Our results indicate that light was not the main direct environmental variable responsible for Q. faginea seedling mortality, but it may be an important indirect fac-tor. In xeric habitats, the recruitment of Q. ilex was greater in shaded than in unshaded microsites because seedlings grew better under partial sunlight, where water stress was reduced (Broncano, Riba & Retana, 1998). �sually, the abundance of grasses is directly driven by openings in the forest canopy, but we did not find a significant relationship

FIgurE 3. Spatial pattern of oak regeneration (small symbols: circles are seedlings; squares are sprouts), adults (filled downward triangles), stumps (empty downward triangles), and C. monogyna individuals in relation to litter cover (empty circles) and herb cover (grey circles) in the study plot. Abbreviations are as in Table II. The size of the circles is directly proportional to the amount of litter or herb cover.

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between these two variables after correcting for the pres-ence of spatial autocorrelation (Table V). Herb cover and light level showed significant positive spatial autocorrela-tion, with patch sizes of 5 and 3 m, respectively. However, the small-scale approach used in this study (1-m2 quadrats) may be unsuitable for revealing a relationship between these two variables in a relatively open stand such as the study site. Light might also arrive diagonally on the forest floor depending on the structure of the understory vegetation (Messier, Parent & Bergeron, 1998).

We detected a significant spatial attraction between C. monogyna and healthy Q. faginea seedlings, which may indicate facilitative effects of this shrub on oak recruit-ment (Callaway, 1992). Li and Wilson (1998) found that contiguous distributions of woody species enhanced woody plant establishment in the mixed-grass prairie of North America. In mesic oakwoods C. monogyna may protect oak seedlings from herbivores (Watt, 1919). Spiny shrubs (e.g., Rubus spp.) did not show any spatial interaction with Q. faginea seedlings at the study site, which suggests that the interaction between C. monogyna adults and healthy Q. faginea seedlings was not related to protection against herbivores. No spatial association was found between adult oaks and C. monogyna, which indicates that indirect effects of trees (e.g., shade) did not explain the association between C. monogyna and healthy oak seedlings. Factors related to

shrub abundance that reduce competition intensity from herbs might also increase the success of oak recruitment (Köchy & Wilson, 2000). However, we did not find any spa-tial relationship between C. monogyna and herb cover, that would suggest indirect effects of this shrub on Q. faginea recruitment. Greater recruitment under shrubs might be also due to higher dispersal rates of acorns (Kikuzawa, 1988), but this does not seem to be the case at the study site, where the main dispersers of C. monogyna fruits (e.g., Turdus spp.) differ from the main acorn consumers (jays, rodents, wild boar). The spatial association between C. monogyna adults and Q. faginea seedlings may be due to favourable microenvironmental conditions provided by the shrub to the oak seedlings, but more specific studies are required to determine if C. monogyna facilitates Q. faginea in sites with Mediterranean climate, as described for other shrub–oak interactions (Rousset & Lepart, 1999).

The studied Q. faginea population expanded by seed-ing and sprouting, which underlines the role of the latter as a form of persistence, whereas recruitment is a means of population replacement (Bond & Midgley, 2001). Sprouting may play an important role for successful persistence of disturbed Q. faginea stands. However, the spatial patterns of Q. faginea sprouts were distributed more regularly than the highly clumped Q. ilex sprouts, which probably originated from the root collar of individuals logged in 1989. These

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y (m

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FIgurE 4. Spatial pattern of oak regeneration (small symbols: circles are seedlings; squares are sprouts), adults (filled downward triangles), stumps (empty downward triangles), and C. monogyna individuals in relation to the available sunlight in the study plot. Abbreviations are as in Table II. The size of the grey circles is directly proportional to the total transmitted radiation.

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patterns indicate that the studied stand was previously dom-inated by Q. ilex, which experienced a selective thinning to enhance the dominance of Q. faginea. Hence, several spatial patterns may appear overlapped as a consequence of the previous disturbance history and the following replacement strategies from a random pattern of seedlings due to seed dispersal and post-establishment competition to a clumped pattern of sprouts. Non-random spatial patterns of regenera-tion also may arise due to the interaction of successive pro-cesses from seed dispersal to establishment.

In conclusion, we found that microsites with dense herb cover showed a greater mortality of Q. faginea seed-lings. We conclude that competition with understory herbs is among the main factors controlling Q. faginea recruit-ment in Mediterranean woodlands. Forest managers should provide measures to control the dominant herbs (e.g., Brachypodium species) in order to increase the performance of oak seedlings in Mediterranean woodlands.

AcknowledgementsWe thank two anonymous reviewers and C. Messier and L.

Sirois for their helpful comments. The 1FD97-0911-C03-01.S�BP1 and RTA2005-00100-C02-00 project and an INIA grant to J. Esteso-Martínez supported this work. We thank L. Alloza, M. A. Pascual, J. J. Peguero-Pina, and S. Sisó for their brave help in the field. J. J. Camarero acknowledges the support of an INIA-Gob. Aragón postdoctoral contract.

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