More than just drought: complexity of recruitment patterns in Mediterranean forests

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OecologiaDOI 10.1007/s00442-014-3064-x

POPULATION ECOLOGY - ORIGINAL RESEARCH

More than just drought: complexity of recruitment patterns in Mediterranean forests

Elena Granda · Adrián Escudero · Fernando Valladares

Received: 7 March 2014 / Accepted: 21 August 2014 © Springer-Verlag Berlin Heidelberg 2014

results pointed to ontogenetic conflicts regarding the seed mass of Q. faginea and to density-dependent seed mortal-ity for Q. ilex, rarely described in Mediterranean ecosys-tems. We propose that our study species experience popula-tion growth in forests dominated by heterospecifics where the recruitment success depends on habitat heterogeneity and on moderated biotic and abiotic stresses created by each species. Our results reveal patterns and mechanisms involved in recruitment constraints that add complexity to the well-known drought-related processes in Mediterranean ecosystems.

Keywords Spatial heterogeneity · Density dependence · Forest dynamics · Seed fate · Summer drought

Introduction

Forests are exposed to recurrent environmental changes which can modify their structure and composition. How-ever, there are mechanisms that maintain ecosystem sta-bility and guarantee species coexistence (Wu and Loucks 1995; González and Loreau 2009; Lloret et al. 2012). Such mechanisms reach their maximum importance during the recruitment stage, as the future forest composition will rely on the regeneration success and performance of the species coexisting in the community (Clark et al. 1999). However, while progress has been made in identifying biotic and abi-otic constraints to regeneration (e.g., McCarthy-Neumann and Kobe 2010; Pérez-Ramos et al. 2012) more empirical studies under natural conditions are still needed to provide a deeper understanding of community functioning and dynamics.

Recruitment constraints are frequent and intense in stressful ecosystems. In many temperate forests, for

Abstract Understanding community dynamics dur-ing early life stages of trees is critical for the prediction of future species composition. In Mediterranean forests drought is a major constraint for regeneration, but likely not the only factor determining the observed spatial pat-terns. We carried out a sowing experiment aimed at iden-tifying main filters during seed-seedling transition. Spe-cifically, we studied seed fate (predation, fungi infection, emergence) and subsequent seedling performance (mor-tality during the first summer and overall recruitment after 2 years) of four co-occurring Mediterranean tree species (Quercus ilex, Quercus faginea, Juniperus thurifera, Pinus nigra). We related these processes to the dominant spe-cies composition, microhabitat heterogeneity, herb cover and seed mass. The identity of the dominant species in the forest canopy was more important for recruitment than the forest canopy being dominated by conspecific vs. hetero-specific species. The patterns we found suggest that biotic interactions such as facilitation (lower mortality under the canopies) and herb competition (during emergence of J. thurifera) are relevant during recruitment. Moreover, our

Communicated by Ines Ibanez.

Electronic supplementary material The online version of this article (doi:10.1007/s00442-014-3064-x) contains supplementary material, which is available to authorized users.

E. Granda (*) · F. Valladares Departamento de Biogeografía y Cambio Global, Museo Nacional de Ciencias Naturales, MNCN-CSIC, Serrano 115 dpdo, 28006 Madrid, Spaine-mail: [email protected]

A. Escudero · F. Valladares Departamento de Biología y Geología, ESCET, Universidad Rey Juan Carlos, Tulipán s/n, 28933 Móstoles, Spain

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instance, these constraints are commonly related to her-bivore or pathogen pressures (e.g., Defossez et al. 2011). However, in the Mediterranean region the prolonged sum-mer droughts coupled with intense irradiances are consid-ered the most limiting factors preventing seedling recruit-ment of newly emerged seedlings (Castro et al. 2004, 2005; Gómez-Aparicio et al. 2005). For this reason, more emphasis has been placed on positive plant–plant interac-tions (i.e., facilitation) as drivers of successful recruitment in Mediterranean forests (Pugnaire et al. 2011). Facilitation has been shown to exert a direct and indirect influence on seedling performance through the modification of abiotic and biotic conditions caused by particular species (Calla-way 1995; Bruno et al. 2003; Cuesta et al. 2010; Holmgren et al. 2012; McIntire and Fajardo 2014). However, while facilitation seems to play a prominent role in plant com-munity dynamics and composition in the Mediterranean region, plant–plant interactions could not fully explain the observed multispecies tree assemblages in a previ-ous study conducted in continental Mediterranean forests (Granda et al. 2012). Thus, we hypothesize that in addi-tion to facilitation involved in reducing water stress, other mechanisms are controlling the complexity of tree recruit-ment and related spatial patterns in Mediterranean forests. For instance, ontogenetic conflicts within early life stages and negative density-dependent responses could also drive recruitment patterns and forest dynamics.

Ontogenetic conflicts have been suggested to be wide-spread in natural systems (Schupp 1995; Pérez-Ramos et al. 2012). Thus, adequate conditions for seed arrival could trans-late into high mortality rates during the following life stages (Schupp 1995). Pérez-Ramos et al. (2012) found a differen-tial influence of optimal seed sizes through ontogeny for two Quercus species in southern Spain, as well as species differ-ences among demographic stages arising from contrasting responses to microhabitat heterogeneity. As a consequence, the study of the seed-seedling transition of coexisting species is necessary to enable a better understanding of the major factors involved in their recruitment process which contrib-ute to long-term species persistence or turnover.

Mechanisms related to density dependence are also proposed to explain species assemblages during recruit-ment in many natural communities (Wright 2002; Peters 2003; Paine et al. 2012). Negative density-dependent mechanisms, including predation, herbivory, competition and fungi or pathogen infection (Janzen 1970; Connell 1971; Chesson 2000), restrict the probability of a seed or a seedling to become a new recruit in the vicinity of con-specifics. These mechanisms promote recruitment away from parent trees and contribute to species coexistence by freeing potential colonization areas for other species under their canopies. However, most studies focused on density dependence have been carried out in species-rich

tropical forests (but see Packer and Clay 2000; HilleRis-Lambers et al. 2002; McCarthy-Neumann and Kobe 2010). Although it has been demonstrated that negative density dependence can be equally important in forests outside the tropical region, in Mediterranean forests it has rarely been addressed.

Our main objectives were to:

1. Identify the main factors involved in the seed-seedling transition of Mediterranean trees and relate them to possible mechanisms controlling overall recruitment.

2. Explore whether ontogenetic conflicts are operating at early life stages.

3. Determine if recruitment constraints are influenced by the conspecific canopy, in accordance with negative density dependence, or favored by a particular hetero-specific canopy.

We expect a lower mortality under the canopies, due to mitigation of abiotic stress, in accordance with most of the relevant studies in the Mediterranean region (e.g., Pug-naire et al. 2011). In addition, we hypothesize that forests differing in species composition cause contrasting habi-tat complexity (McIntire and Fajardo 2014) that will favor the recruitment of some species over others depending on pathogen and predation pressures, as well as on seedling physiological tolerances. In fact, the species identity of the dominant adults is expected to have a greater effect on suc-cessful recruitment than the influence of conspecific vs. het-erospecific canopy (Webb et al. 2006). We further predict that ontogenetic conflicts might occur (Pérez-Ramos et al. 2012), especially across some microhabitats and/or life stages (e.g., higher emergence in gaps but lower subsequent seedling performance). Through the assessment of post-dis-persal seed fate and subsequent seedling performance under natural conditions, we were able to identify the main filters occurring during the seed-seedling transition and relate them to the complexity of recruitment patterns.

Materials and methods

To address the objectives described above we:

1. Studied seed fate through the quantification of seeds that died, were predated or emerged as seedlings in forests differing in the dominant species identity of the adults (forest types) and at two levels of microhabitat heterogeneity (canopies and gaps).

2. Studied subsequent seedling performance by identify-ing the period, location and causes of mortality dur-ing the first summer and final survival after more than 2 years (i.e., overall recruitment).

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Study area and species

The study area is located in the Alto Tajo Natural Park, in central Spain (Guadalajara, Castilla-La Mancha; 40º40′51″N, 02º04′31″W). The climate is continental Mediterranean with hot and dry summers and cold winters, with a mean annual temperature of 10.2 °C and a mean annual precipitation of 490.8 mm (Spanish Meteorological Agency, Molina de Aragón weather station, 1951–2012). The soils are poorly developed and formed mainly from Cretaceous and Jurassic limestones.

We selected four coexisting and abundant tree species in the region: an evergreen oak, Quercus ilex subsp. ballota (Desf.) Samp.; a semi-deciduous oak, Quercus faginea Lam.; and two conifers, Pinus nigra Arn. subsp. salzmannii (Dunal) Franco and Juniperus thurifera L. Each species is dominant in certain locations of the study area but the other three tree species commonly coexist in all the forest stands simply vary-ing in their local abundance. Seeds of the four species were collected in the field and used in our experimental design.

Potential seed consumers in the study area are rodents (Mus spretus, Apodemus sylvaticus and Oryctolagus cunic-ulus), birds (Garrulus glandarius and Turdus spp.), ungu-lates (Sus scrofa, Capreolus capreolus and Cervus ela-phus), cattle (mainly sheep, Ovis aries), small carnivore mammals (Vulpes vulpes and Martes foina), filbert worm (Cydia spp., Tortricidae) and filbert weevil (Curculio spp, Curculionidae). Quercus seeds are dispersed by the above-mentioned rodents and birds (Gómez 2003; Pulido and Díaz 2005) and Juniperus seeds by rodents, birds, cattle and small mammals through seed deposition (Santos et al. 1999; Escribano-Ávila et al. 2012).

Experimental design

We performed a sowing experiment in an ecosystem com-posed of forests with similar climatic conditions and parent rock material but differing in the identity of the dominant spe-cies in the canopy. This study system allows us to emphasize the role of factors that differ from the macroclimatic ones to assess recruitment constraints. The sowing experiment was carried out following a factorial design [see scheme in Elec-tronic supplementary material (ESM) Fig. S1]. We selected four forest types determined by the dominant tree species: (1) Q. ilex forests (Qi-F), (2) Q. faginea forests (Qf-F), (3) P. nigra forests (Pn-F), and (4) J. thurifera forests (Jt-F). We con-sidered a species to be dominant when it surpassed 80 % of the forest cover. Sowing points were distributed in two stands per forest type. The eight forest stands were separated by more than 2 km and they were chosen to present similar slope (flat-ter than 5 %), parent rock material, altitude, annual precipita-tion and temperatures (see ESM Table S1). Each stand con-sisted of three plots with four replicates of two microhabitats,

which correspond to distinct ground heterogeneity levels: canopy (under the projection of the dominant tree species at each type of forest) and gap (open spaces). Twenty seeds per species (Q. ilex, Q. faginea, P. nigra and J. thurifera) were sown in 40 × 50-cm subplots at each microhabitat, giving a total of 15,360 sown seeds (3,840 seeds per species, 4 types of forests × 2 forest stands × 3 plots × 4 sites × 2 microhabi-tats × 20 seeds; see ESM Fig. S1). As a consequence of the lack of P. nigra emergence, we do not show field results for regeneration of this species.

Seed collection and sowing procedure

Seeds of Q. ilex and Q. faginea were collected in October–November 2008 from 65 to 75 randomly selected trees covering all the study area (30–200 harvested seeds per mother tree). Seeds were surveyed to discard the aborted, dried and infected ones, and individually weighed and marked. Mean ± SD seed weight (g) was 2.19 ± 0.79 and 2.51 ± 0.76 for Q. ilex and Q. faginea, respectively. Seeds were soaked for 24 h before being sown; floating seeds were removed. In December 2008, seeds were sown in the field at 2 to 4-cm depth, separated by 10 cm from each other and in a horizontal position to simulate burial by the Eurasian jay Garrulus glandarius (Bossema 1979; Gómez 2003), the most abundant genuine disperser in the study area. Seeds from J. thurifera were collected in Octo-ber 2008 and seeds of P. nigra in January 2009 from 20 different trees in the study area. J. thurifera seeds were sub-jected to stratification treatments following García-Fayos et al. (2008). Mean ± SD seed weight (g) was 0.04 ± 0.006 and 0.02 ± 0.004 for J. thurifera and P. nigra, respectively. The two conifer species were sown in April 2009, coincid-ing with their natural dissemination period in the field; the same protocol was followed as for Quercus seeds.

At the same time that sowing was being carried out in the field (December 2008 for Quercus species and April 2009 for conifer species), 160–200 seeds per species (distributed in 16 different trays, four per species), were also sown under opti-mal controlled conditions in germination chambers (20 °C at 50 % air humidity, always maintaining the substrate humid). Emergence in the chambers was monitored every week for 2–3 months for Q. ilex, Q. faginea and P. nigra. In the case of J. thurifera, seeds were maintained in the chambers for 6 months, as seedlings started to emerge after 4–5 months. Seedling emergence under controlled conditions resulted in high rates for Q. ilex (95 %), Q. faginea (96 %) and P. nigra (89 %), while J. thurifera showed only a 3.5 % emergence.

Seed and seedling monitoring

From the sowing date until the end of the summer 2009, all sowing sites were visited every month. After the first

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summer, the sites were visited in November 2009, Sep-tember 2010, June 2011 and finally in September 2011 (980 days after Quercus seeds were sown and 900 after sowing conifer seeds). During the whole study period we monitored (see scheme in ESM Fig. S2) seed predation in situ (whenever we found the remains of eaten seeds that could be attributable to rodents or wild boar), seedling emergence and mortality (due to browsing or drought). In November 2009 we unburied the non-emerged Quercus seeds and classified them as: dead seed (mainly caused by fungus), or removed seed without a known agent (non-found seed). Seeds of J. thurifera and P. nigra were not unburied due to their small size. No insect and/or disease damage was observed in the seedlings of the study species. Percentage of herb cover was visually estimated with pho-tographs taken perpendicularly at each subplot during the spring of 2011.

Rodent sampling and presence of feces

A 3-night trapping session was carried out in February 2009 during the new moon. Throughout these 3 consecu-tive nights, 49 traps were set 10 m apart at each forest stand (two forest stands per type of forest) making a total of 392 traps. Rodents were identified to species, weighed, marked and released [see Muñoz and Bonal (2007) and Torre et al. (2007) for further details on the protocol]. Feces of rodents, cattle and ungulates in a circle of 1-m radius centred in each trap were also surveyed in February.

Statistical analyses

We built contingency tables summarizing the frequency of: (1) seed fate, i.e., frequency of seeds that turned into emerged seedlings (emergence), died (mortality) or were predated (pre-dation); (2) seed predation by different agents, i.e., frequency of removed seeds (non-found), eaten in situ by rodents or by wild boar; and (3) causes of seedling mortality, i.e., fre-quency of dry or browsed seedlings at different types of for-ests. These contingency tables were analyzed for each species using log-linear models, where the null hypothesis was that the frequency of each response was independent of the for-est type. The log-linear models fit the expected cell counts to the marginal sums of the contingency table (see Agresti 1996; Gotelli and Ellison 2004). Deviations from expected frequen-cies were displayed and explored with mosaic plots (Friendly 1994). The mosaic plot is a graphical method for visualizing contingency tables and for building models to account for the associations among its variables (Friendly 1994, 1999). Seed predation and mortality of conifers were not included in these analyses as the small size of these seeds did not allow us to find them in the field. Analyses were performed using R soft-ware version 2.15.1 (R Development Core Team 2012).

Generalized linear mixed effect models (Pinheiro et al. 2000) with binomial distributions were used. The response variables were: seed predation (removed seeds and those eaten in situ from the sown ones); seedling emergence (i.e., seedlings which emerged from the non-predated seeds), seedling mortality (i.e., emerged seedlings which died after the first summer) and overall recruitment (i.e., seed-lings from the total number of sown seeds which survived for more than 2 years). We built two sets of models per response variable and species. The first set was composed of the explanatory variables seed mass and herb cover as covariates, forest type, microhabitat and their interaction as fixed effects. The second set substituted “forest type” by “conspecificity vs. heterospecificity” of the dominant spe-cies in the canopy. Random effects were site, plot and for-est stand properly nested. The model with the best subset of predictors for each response variable was selected by com-paring the Akaike´s information criterion (Burnham and Anderson 2002). These analyses were performed using the package lme4 (Bates and Maechler 2010) in the R software version 2.15.1 (R Development Core Team 2012).

We used the Kaplan–Meier estimates to obtain the mor-tality functions of each species. We performed a χ2 mul-tiple comparison test to check for significant differences among forest types. Afterwards, log-rank tests were used to test for differences in the corresponding curves for all pos-sible pair-wise combinations (Pyke and Thompson 1986). These analyses were performed using STATISTICA 6.0 (Statsoft, Tulsa, OK).

Results

A total of 903 Q. ilex, 875 Q. faginea and 131 J. thurifera seedlings emerged, of which 385 (43 %), 268 (31 %) and 72 (55 %), respectively, were alive at the end of the study. Thus, 10, 6.9 and 1.8 % represented the overall recruitment percent (i.e., individuals that survived for more than 2 years from the total number of sown seeds) of Q. ilex, Q. faginea, and J. thurifera, respectively (see ESM Table S2 for further details). P. nigra did not emerge in the field. As a conse-quence, results for this species are only provided for con-trolled conditions in the growth chambers.

Seed fate: mortality, predation or emergence

Significant differences were detected in the frequencies of seed mortality, predation and seedling emergence in each forest type for Q. ilex (χ2 = 666, df = 6, P < 0.0001) and Q. faginea (χ2 = 675, df = 6, P < 0.0001) as indicated by the log-linear models (Fig. 1). The highest seed mortality for Q. faginea, mainly attributable to fungi, was found in for-ests dominated by P. nigra (Pn-F; Fig. 1b). By contrast, in

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agreement with the density-dependence theory, in the case of Q. ilex the mortality of seeds caused by fungus infection was found to be higher than expected in forests dominated by conspecifics. Although the number of infected Q. ilex seeds was not very high, positive and significant deviations (α = 0.0001) were found from the expected cell frequen-cies in Qi-F (Fig. 1a).

Predation rates did not depend on whether the forest was conspecific or heterospecific but on the identity of the dominant species in the canopy (i.e., forest type): preda-tion was significantly higher than expected in the Qf-F and, more importantly, in Jt-F for both Quercus seeds (Fig. 1; Table 1). In contrast, lower seed predation was found in Pn-F and Qi-F. Heavier seeds of Q. faginea were more

predated, while those of Q. ilex experienced less preda-tion (Table 1). Of all the predated seeds, the removed ones (probably a high percentage consumed by large herbivores and cattle) were more abundant than the ones eaten in situ by wild boar or rodents. Seed removal was significantly higher than expected in the forests with the highest pre-dation rates (Qf-F and Jt-F, see ESM Fig. S3). Wild boars were responsible for seed predation with a higher fre-quency than expected in Qi-F and Pn-F, but not in Qf-F and Jt-F, in spite of their recorded presence in such forests (see ESM Fig. S3, Table S3). Rodents were found to predate more seeds in Pn-F for Q. faginea and in Jt-F for Q. ilex. However, low rodent abundance was found in the study area, with only 11 captured rodents (see ESM Table S1).

Total emergence in the field was 23.5, 23.2, 3.41 % for Q. ilex, Q. faginea and J. thurifera, respectively (see Table S2 for total abundance). All P. nigra seeds and/or seedlings died before we were able to record any emergence. In the field, emergence of both Quercus species depended on the forest type due to the predation rates (Fig. 1), but not to dif-ferent conditions for emergence provided by each forest. In fact, when considering the emergence of the non-predated seeds (Table 1) we observed that the seed mass was the only important variable for emergence of Quercus species, where heavier seeds had higher emergence for Q. ilex and lower emergence for Q. faginea. Emergence of J. thurifera was first recorded in September of 2010. Overall, the emer-gence for this species was very low and negatively influ-enced by herb cover (Table 1). None of the study species showed significant differences in emergence depending on the conspecificity vs. heterospecificity of the dominant spe-cies (Table 1).

Seedling mortality during the first summer: timing and causes of death

We found that after the first summer, seedling mortal-ity was significantly higher in the gaps than in the cano-pies for the three study species (Table 1). Both Quercus species experienced increased mortality of seedlings originating from smaller seeds (Table 1). In the case of Q. ilex, mortality also depended on the forest type and on the interaction Forest type × Microhabitat, but it was not significantly related to conspecific-heterospecific canopy (Table 1b). Mortality curves differed among forest types for all species: Q. ilex (χ2 = 34.6, df = 3, P < 0.0001), Q. faginea (χ2 = 62.4, df = 3, P < 0.0001) and J. thurifera (χ2 = 7.6, df = 3, P = 0.05), but in all forests mortality rates increased from the beginning of the summer season (first summer after emergence; Fig. 2). Juniper forests had the highest rates of mortality for both Quercus species, and at the end of the study period (September 2011, 980 days after sowing) all seedlings of Q. ilex and Q. faginea had

Fig. 1 Fate of seeds of a Quercus ilex and b Quercus faginea sown in four forest types: Q ilex forest (Qi-F), Q. faginea forest (Qf-F), Pinus nigra forest (Pn-F) and Juniperus thurifera forest (Jt-F). The area of each rectangle is proportional to the cell frequency of the corresponding contingency table. The shading of each rectangle is proportional to standardized residuals from the fitted model (values indicated in the legend). White rectangles indicate non-significant deviations from the expected cell frequencies, gray rectangles indi-cate significant deviations at ca. α = 0.05, black rectangles indicate significant deviations at ca. α = 0.0001. Solid lines designate positive and broken lines negative deviations from the expected frequencies

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Tabl

e 1

Res

ults

of

the

gene

raliz

ed li

near

mix

ed m

odel

s fo

r th

e ef

fect

s of

for

est t

ype

(Que

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ile

x fo

rest

s, Q

uerc

us f

agin

ea f

ores

ts, P

inus

nig

ra f

ores

ts, J

unip

erus

thu

rife

ra f

ores

ts),

mic

roha

bi-

tat [

cano

py (

C)

and

gap

(G)]

, her

b co

ver

and

seed

mas

s on

: see

d pr

edat

ion,

see

dlin

g em

erge

nce,

mor

talit

y af

ter

the

first

sum

mer

and

ove

rall

recr

uitm

ent o

f ea

ch s

peci

es

Res

ults

obt

aine

d by

rep

laci

ng “

fore

st ty

pe”

by th

e “c

onsp

ecifi

c vs

. het

eros

peci

fic”

natu

re o

f th

e ad

ult c

anop

y ar

e al

so s

how

n fo

r co

mpa

riso

n [c

onsp

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c (Y

)]. M

odel

sel

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as c

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by

Aka

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s in

form

atio

n cr

iteri

on (

AIC

). V

alue

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ΔA

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ify

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mag

nitu

de o

f di

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bet

wee

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e nu

ll m

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(in

terc

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only

mod

el)

and

the

mod

el w

ith th

e lo

wes

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(be

st m

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). T

he

vari

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s in

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ed in

the

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are

thos

e sh

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in th

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ble,

for

whi

ch w

e pr

ovid

e th

e si

gn o

f th

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timat

es (+

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d χ

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tistic

Sign

ifica

nce

leve

ls (

* P

< 0

.05,

**

P <

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1, *

** P

< 0

.001

) of

the

χ2 -t

est i

ndic

ate

a si

gnifi

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ly w

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fit o

f th

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odel

with

out t

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Mod

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ΔA

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mas

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AIC

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spec

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(C

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habi

tat

(M)

C ×

MH

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co

ver

See

d m

ass

Pred

atio

nQ

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x18

7.14

*–

––

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***

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––

––

(−

)18.

92**

*

Q. f

agin

ea71

.112

.06*

*–

––

(+)6

7.04

***

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––

––

(+

)67.

04**

*

Em

erge

nce

of

non-

pred

ated

se

eds

Q. i

lex

3.44

––

––

(+)5

.44*

3.4

––

––

(+)5

.44*

Q. f

agin

ea14

.85

––

––

(−)1

6.85

***

14.8

––

––

(−)1

6.85

***

J. th

urif

era

7.7

––

–(−

)9.7

2**

–7.

7–

––

(−)9

.72*

*–

Mor

talit

y af

ter

fir

st s

umm

erQ

. ile

x53

.340

.34*

**(+

G)6

3.03

***

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9***

–(−

)4.8

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.9–

(+G

)26.

19 *

**–

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.2–

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)23.

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*–

–(−

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*44

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)23.

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4.6

11.6

5*(+

G)1

3.99

**7.

06*

––

6.02

(+Y

)7.0

9**

(+G

)3.0

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––

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rall

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uitm

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(out

of

tota

l nu

mbe

r of

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n

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s)

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lex

45.5

23.8

***

(+C

)31.

37**

*9.

65*

–(+

)14.

89**

*33

.7–

(+C

)22.

54**

*–

–(+

)15.

17**

*

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agin

ea39

.312

.89*

*(+

C)9

.55*

*–

–(+

)26.

2632

.4–

(+C

)9.6

9**

––

(+)2

6.23

***

J. th

urif

era

11.3

–(+

C)5

.89*

–(−

)9.0

9**

–11

.3–

(+C

)5.8

9*–

(−)9

.09*

*–

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died in the gaps of these forests (see ESM Table S2). Mor-tality of J. thurifera was generally low at the end of the first summer (after 900 days from the sowing date; Fig. 2c), but it was significantly higher in the gaps than in the canopies (Table 1). J. thurifera seedling mortality also depended on the forest type, being the only species for which mortality was higher in forests dominated by conspecifics (Table 1).

The main causes of seedling mortality of each species significantly varied among forest types (χ2 = 26.55–65.37, df = 3, P < 0.0001). Interestingly, the three study species

Fig. 2 Seedling mortality in different forest types over the first grow-ing season for a Q. ilex (sown in December 2008), b Q. faginea (sown in December 2008) and c J. thurifera (sown in April 2009). For abbreviations, see Fig. 1

Fig. 3 Percentage of sown seeds surviving to different life stages: a Q. ilex, b Q. faginea and c J. thurifera in two microhabitats (canopy and gap) and four forest types. Sources of mortality for different life history stages are indicated. For abbreviations, see Fig. 1

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presented different mortality patterns (see ESM Fig. S4). Drought caused higher mortality in Jt-F for Q. ilex and in Qf-F for Q. faginea. Lower frequency of dry seedlings was found in Pn-F for Q. ilex and in Qi-F for Q. faginea (ESM Fig. S4a, b). However, not all seedlings died as a conse-quence of drought: intensive browsing, mainly by rabbits that ate the tender shoots at the base (see ESM Fig. S2; Fig. S4; Table S3) was found in Qi-F for both Quercus species and also in Pn-F for Q. ilex seedlings. Most dead seedlings of J. thurifera were found dry at all forest types. Only in Qi-F some browsed seedlings of this species were found (ESM Fig. S4c).

Overall recruitment

None of the study species showed better performance and overall recruitment after more than 2 years in forests where conspecifics were dominant (Fig. 3). Overall recruitment (recruited seedlings from the sown ones) at the end of the study period indicated that the evergreen holm oak, Q. ilex, had the highest regeneration rates at all forest types (Fig. 3; see ESM Table S2) followed by the deciduous Q. faginea, and the conifer J. thurifera. Seed mass had an overall positive effect on regeneration for the Quercus species (Table 1). The microhabitat also played an important role on overall recruitment for all species, being higher under the canopies than in gaps. Further, forest type had a remark-able influence on Quercus species, as has been previously shown: Q. ilex recruited better in Pn-F due to a combina-tion of lower predation and lower seedling mortality; Q. faginea also recruited better in Pn-F, mainly as a conse-quence of lower seed predation; and J. thurifera recruited better where herb cover was lower (Table 1; Fig. 3). None of the species showed significant differences in recruitment after more than 2 years between forests dominated by con-specifics vs. heterospecifics (Table 1; Fig. 3; ESM Table S2).

Discussion

Our study shows the main post-dispersal factors involved in the seed-seedling transition and related mechanisms that modulate the species composition in these continen-tal Mediterranean forests. While increased survival under the canopies indicated the importance of reducing drought stress for successful recruitment, other complex factors rarely studied in the Mediterranean region were involved. These included contrasting effects of the dominant species identity; the effect of seed mass, which varied according to the life stage of the individuals indicating ontogenetic con-flicts within early life stages and patterns suggesting den-sity dependence.

Main filters during recruitment differ among species and early life stages

Post-dispersal seed predation and seedling mortality were the most limiting factors during recruitment for both Quercus species, while the emergence stage was more criti-cal for J. thurifera.

Post-dispersal predation of Quercus seeds was dependent on the identity of the dominant species in the forest canopy (forest type), while seedling performance after emergence was mainly determined by microhabitat heterogeneity. Seed predation did not differ between canopies and gaps, which could be a consequence of high seed predation by ungu-lates and cattle, whose foraging patterns are less selective than those of rodents, as has been previously found (Gómez et al. 2003; González-Rodríguez and Villar 2012). The high-est predation rates were found in juniper forests, where most seeds were removed. It is possible that a fraction of these removed seeds could have been secondarily dispersed by rodents or jays (Pulido and Díaz 2005; Perea et al. 2011), favoring their redistribution and ability to colonize new areas. However, the high seed predation in these forests is probably due to soil frost heave (also described by Cas-tro et al. 2004), which pulled up the buried seeds making them accessible for all seed consumers (personal observa-tion). Earlier studies have proposed that spatial variation in post-dispersal seed predation may promote species coex-istence (Hulme 1998; Pérez-Ramos et al. 2008; González-Rodríguez and Villar 2012). Similarly, our results suggest that the lowest predation rates found in pine forests for both Quercus species could contribute to enhanced recruitment of these species. The low predation found in pine forests is likely a consequence of the combined effect of low cattle pressure and low seed availability in these forests that attract fewer predators and reduce the time that they spend looking for food (Schupp 1995; Gómez and Hódar 2008).

The effect of seed mass on each response variable depended upon the oak tree species and the life stage con-sidered, but from an overall perspective heavier seeds of both Quercus had a higher probability of recruitment. A positive effect of seed size on most fitness components related to seedling establishment is commonly found (but see Gómez 2004; González-Rodríguez et al. 2012). Larger seeds allocate more resources to root systems, which allow a more efficient use of water and nutrients, favoring seed-ling performance and survival (Lloret et al. 1999). While Q. ilex seedlings originating from heavier seeds performed better during all life stages, Q. faginea showed ontogenetic conflicts. These results are in accordance with previous studies reporting ontogenetic conflicts in other Mediter-ranean ecosystems (Pérez-Ramos et al. 2008, 2012). The seed mass of Q. faginea was positively related to preda-tion, probably because large acorns are preferred by the

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main post-dispersal seed consumers (Gómez 2004). How-ever, low seedling mortality after the first summer of heav-ier seeds resulted in enhanced overall recruitment for Q. faginea, as occurred in Q. ilex.

The emergence stage was less crucial for overall recruit-ment of Quercus species, compared to the seed predation stage and seedling mortality. Regarding J. thurifera we found that the patches with fewer herbs were safer sites for the emergence and overall recruitment [see also Maes-tre et al. (2004) for the Mediterranean shrub Pistacia len-tiscus]. In contrast, Quercus species showed higher herb competition tolerance than J. thurifera, allowing seedling regeneration over a wider area (Kunstler et al. 2006). Nev-ertheless, further research is needed to confirm these find-ings given that J. thurifera emergence was scant and that herb competition may change during different climatic con-ditions, as found by Cuesta et al. (2010).

In accordance with other studies in Mediterranean eco-systems, seedling mortality was very high during the first summer for all species (Escudero et al. 1999; Castro et al. 2005; Pugnaire et al. 2011). Overall, drought was the main cause of mortality, even though browsing was also impor-tant in some forest types. We found a disproportionally higher survival of seedlings under tree canopies compared to gaps, suggesting that facilitation plays an important role in recruitment by improving the chances of survival during the critical first summer drought. Possible mecha-nisms are likely related to an amelioration of abiotic stress and increased access to resources due to lower light levels and higher water or nutrient availability under the canopies (Castro et al. 2004; Gómez-Aparicio et al. 2005; Holmgren et al. 2012). Forests dominated by J. thurifera displayed the highest mortality rates, probably due to their low tree cover (Table S1), which allows excessive irradiances. We propose that these high irradiances coupled with the intense summer drought exacerbated the negative impact of drought, reduc-ing seedling performance (Holmgren et al. 2012), with differences among species depending on their shade and drought tolerances (Gómez-Aparicio et al. 2006; Flexas et al. 2014). Indeed, the percentage of surviving seedlings (ESM Table S2) after the first summer in juniper forests was highest for J. thurifera followed by Q. ilex and Q. faginea, coinciding with the water stress tolerances of these (or related) species (Flexas et al. 2014). This high mortal-ity could be also associated with the fact that the shallow roots of juniper adults (Castillo et al. 2002) might decrease the availability of soil water from the superficial soil lay-ers, and thus may compete with seedlings whose roots are not deep enough to access soil water from deeper layers. Surprisingly, the percentage of surviving seedlings after the first summer for J. thurifera was very high, meaning that even though the emergence was scant, once emerged these individuals have a high probability of recruitment.

The importance of the species identity of dominant adults

According to the hypothesis of negative density depend-ence we would expect an inverse relationship between conspecific adult dominance and individual performance (Chesson 2000). Instead, the observed responses highlight that seed fate and seedling performance were not deter-mined by the dominance of conspecifics vs. heterospecif-ics, but by the identity of the species dominating the can-opy. The dominant species identity has already been shown to play a significant role in the invasibility of grasslands by trees (Emery and Gross 2007) and in the diversity of tropi-cal forests (Uriarte et al. 2004). Similarly, we argue that in Mediterranean forests the species identity of the individu-als dominating the canopy is crucial for forest dynamics. Because forests were selected for similar climatic condi-tions and parent rock material, we suggest that the contrast-ing seedling performance in different forest types is related to the habitat complexity created by the physical presence of particular adult species [e.g., light quality or variation in evapotranspiration (see McIntire and Fajardo 2014)]. As a consequence, partitioning into conspecific and het-erospecific canopy, commonly found in the literature, may obscure the effects of the great variation that species iden-tity can offer (see also Webb et al. 2006).

Despite the general pattern, we found two exceptions that emphasize the fact that negative density-dependent processes could also modulate coexistence in Mediterra-nean forests. Firstly, we found that fungi were responsible for seed mortality in forests where conspecifics were dom-inant for Q. ilex. As a result, in the long term, this negative density dependence could promote species coexistence if infection of the most common species favors the estab-lishment of other species. Our results do not allow us to demonstrate whether these fungi are host-specific natural enemies. However, the fact that fungi did not affect coex-isting Q. faginea seeds in Qi-F could suggest their speci-ficity for Q. ilex, in accordance with the Janzen-Connell hypothesis (Janzen 1970; Connell 1971). Further research is needed, including the study of non-random patterns of pathogens and their effects on plant community dynamics (Gómez-Aparicio et al. 2012), and through experiments using fungicide treatments (Packer and Clay 2000). Sec-ondly, we found higher mortality after the first summer of J. thurifera seedlings in forests dominated by conspe-cifics (Table 1b). This result could correspond to density-dependent mortality, although the fact that the other spe-cies also experienced high mortality rates in these forests suggest that other factors such as higher irradiances or reduced water availability might be involved in the mortal-ity patterns. Above all, we emphasize the knowledge gap of negative density-dependent processes in Mediterranean forests.

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To conclude, the fact that none of the study species showed a higher overall recruitment in forests dominated by conspecifics, together with a previous observational study showing that juveniles were not spatially associ-ated with conspecific adults (Granda et al. 2012), suggest the prelude of dominant species turnover within forests. At the ecosystem level, instead, we expect coexistence to be maintained due to dynamic species turnover in patches of different forest types that cancel each other out at regional or landscape levels (Wu and Loucks 1995). Moreover, we demonstrate that studies dividing species into conspecifics and heterospecifics obscure the great variation in the effects of each particular canopy species (Webb et al. 2006). Indeed, not only the identity of the dominant neighbors and the influence of facilitation but also complex processes including density dependence and other biotic interactions coupled with ontogenetic conflicts are suggested to be responsible for Mediterranean tree recruitment patterns and coexistence. Our results illustrate the relevance of a suite of processes during the seed–seedling transition that add complexity to the recruitment constraints solely induced by drought in Mediterranean ecosystems.

Acknowledgments We are very grateful to Mario Díaz for assis-tance in rodent sampling, Sasha Wright for comments on statisti-cal methods and to all the people who helped in the field, especially David López and Gonzalo Caballé. We also thank the Junta de Castilla-La Mancha, the director and park rangers of the Alto Tajo Natural Park for permission and facilities provided. We thank the edi-tor and the anonymous reviewers for their constructive comments, which helped us to improve the manuscript. The experiments com-ply with the current laws of the country (Spain) in which the experi-ments were performed. This work was supported by the Spanish Ministry for Innovation and Science with the grants FPI (CGL2007-66066-C04-02) to E. G., Consolider Montes (CSD2008 00040), VULGLO (CGL2010 22180 C03 03) and MOUNTAINS (CGL-2012-38427), and by the Community of Madrid grant REMEDINAL 2 (CM S2009 AMB 1783).

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