Journal of

Ecology 2000,
Recruitment dynamics of a ¯eshy-fruited plant (Olea
88, 622±633 europaea): connecting patterns of seed dispersal to
seedling establishment
PEDRO J. REY and JULIO M. ALCAÂ NTARA
Departamento de BiologõÂa Animal, Vegetal y EcologõÂa, AÂrea de EcologõÂa, Universidad de JaeÂn, E-23071 JaeÂn,
Spain

Summary
1 Little is known about the consequences of seed-disperser activity for plant demo-
graphy. We compared the spatial patterns of seed dispersal generated by frugivor-
ous birds with those of seedling survival for the shrub Olea europaea. We examined
the relative importance of dispersal in determining plant recruitment and tested
whether the initial dispersal pattern persisted throughout recruitment.
2 We quanti®ed the processes a€ecting each stage of regeneration (seed within a
ripe fruit, dispersed seed, seedling and sapling) in di€erent microhabitats, and eval-
uated transition probabilities between stages. We could then determine the overall
probability of a seed in a ripe fruit becoming a sapling, and compare the probabil-
ity of such an event occurring in di€erent microhabitats.
3 Only 9.3% of the emerged seedlings reached the sapling stage, whereas 35.3% of
the seeds were dispersed; 27.0% of dispersed seeds produced seedlings and 62.9%
of saplings survived for 2 years. Seedling survival was therefore the critical link in
regeneration. Water stress was responsible for more than 70% of seedling losses,
which suggests that abiotic factors (mainly rainfall) may account for most of the
¯uctuation in recruitment in this species.
4 Neither post-dispersal seed predation nor germination caused changes in the
initial spatial distribution of seeds, but di€erences in the requirements of seeds and
seedlings then caused spatial uncoupling. The most favourable places for seeds
were the worst for seedlings, and consequently frugivore-generated dispersal pat-
terns di€ered from the ®nal spatial pattern of recruitment.
5 Recruitment under conspeci®cs was nearly zero and dispersers are therefore cru-
cial if recruitment is to occur. Their e€ect on the amount of recruitment was, how-
ever, overwhelmed by processes acting on the seedling stage.
6 For Olea europaea, the pattern generated by short-term recruitment dynamics
persists in the long-term spatial distribution of saplings.

Key-words: avian-seed dispersal, biotic and abiotic factors, microhabitats, plant

recruitment, seed±seedling con¯icts
Journal of Ecology (2000) 88, 622±633

Introduction 1995). Over the last two decades, most studies of

Seed dispersal is a key process in plant population
dynamics (Harper 1977). Although it is implicitly
assumed that animal dispersers can in¯uence plant
population dynamics, their role has seldom been
evaluated (Estrada & Fleming 1986; Jordano 1992;
Willson 1992; Fleming & Estrada 1993; Herrera
# 2000 British Correspondence: Pedro J. Rey (tel. ‡34 953212145; fax
Ecological Society ‡34 953212141; e-mail prey@ujaen.es).
seed dispersal have focused on just one of the sev-
eral stages leading to recruitment (but see Herrera
et al. 1994; Houle 1998; Clark et al. 1999).
Conclusions about the evolutionary and ecological
importance of dispersers may therefore be limited
by an absence of information about the remaining
stages (Schupp 1995; Schupp & Fuentes 1995). If
however, we view dispersal as one event within a
sequence, it is possible to determine the relative
importance of dispersers in driving recruitment
623 dynamics by contrasting their e€ect with subsequent
P. J. Rey & interactions.
J. M. AlcaÂntara The result of recruitment in heterogeneous habi-
tats can be expressed in terms of the number and
spatial distribution of new individuals incorporated
into the population, both of which can be in¯uenced
by seed dispersers. Dispersers can limit recruitment
if the probability of a seed being dispersed is lower
than the probability of a dispersed seed becoming
an established plant. However, ¯eshy-fruited trees
usually produce large crops that are dispersed by a
coterie of animal species (Jordano 1992; Herrera
1995), and we therefore hypothesize that dispersal is
unlikely to be the limiting process in the recruitment
dynamics of such species.
Nevertheless, dispersers may disseminate di€erent
numbers of seeds in a variety of microhabitats, and
thus either shape the spatial distribution of the seed-
lings or limit recruitment by depositing large num-
bers of seeds in places that are unsuitable for
recruitment. Processes acting at di€erent recruitment
stages are likely to be independent and evidence of
such `uncoupling' (Jordano & Herrera 1995) would
indicate the complexity of selective forces in play
during the life cycle of the plant, including seed±
seedling con¯icts (Schupp 1995). Di€erent outcomes
for each stage in di€erent microhabitats (spatial dis-
cordance, Jordano & Herrera 1995) are partly a
consequence of uncoupling because the recruitment-
driving processes, which may have a strong e€ect on
spatial pattern, can vary between microhabitats
(Shibata & Nakashizuka 1995; Houle 1998). We
hypothesize that the spatial pattern of recruitment
will initially be established by seed dispersers but
may then be altered by uncoupling and spatial dis-
cordance (Schupp 1995; Schupp & Fuentes 1995).
We use a demographic approach to explore our
hypotheses linking seed dispersal to recruitment in
Olea europaea var. sylvestris. Brot. (wild olive, here-
after Olea), a Mediterranean bird-dispersed tree. We
use a simple model of the plant life cycle, composed
of life stages connected by transition probabilities
(Harper 1977; Jordano & Herrera 1995) that are
determined by a number of processes. A process is
any event that a€ects the probability of a propagule
moving from one stage to the next: pre-dispersal
seed loss (whereby the seed fails to reach the dis-
persed seed stage) is a process and may be caused
by biotic factors, like granivorous insect larvae, or
by abiotic factors, such as frost. Our approach is
exploratory rather than predictive. We analyse the
in¯uence of biotic and abiotic factors on each
recruitment stage (pre-dispersed seed, dispersed
seed, seedling and sapling), and then estimate the
transition probabilities (hereafter TP) between
stages and the overall probability of a seed in a ripe
# 2000 British
fruit becoming an established juvenile plant (i.e.
Ecological Society
Journal of Ecology, overall probability of recruitment, hereafter OPR).
88, 622±633 Comparison of TPs and OPRs between microhabi-
tats allows us to explore the extent and in¯uence of
spatial discordance, and, by analysing each process,
to determine which one in¯uences the ®nal spatial
pattern and dynamics of recruitment.
Our design allows us to address some of the most
relevant and current questions concerning the link
between seed dispersal and recruitment (see, e.g.
Jordano & Herrera 1995; Schupp & Fuentes 1995;
Schupp 1995; Houle 1998; Clark et al. 1999); speci®-
cally: (i) which are the critical life stages and pro-
cesses in recruitment, (ii) how do processes
operating at di€erent stages interact to a€ect ®nal
recruitment patterns, (iii) are the best sites for seeds
also the best for seedlings, i.e. is seed±seedling con-
¯ict in operation, and (iv) does the activity of seed
dispersers determine the spatial distribution of
recruitment, or is it counteracted by the existence of
strong spatial discordance?
Methods
STUDY SPECIES AND STUDY AREA
Olea grows along the northern Mediterranean basin
and bears hermaphrodite ¯owers (4±6 mm in dia-
meter), from late April to mid June, in axillary
racemes on the previous year's wood. Pollination is
anemophilous with partial self-compatibility
(FernaÂndez 1979). Functional dioecy, through some
individuals expressing only male function, has been
suggested (Jordano 1987). The fruits are drupes that
ripen in autumn and winter, and contain a single
seed dispersal unit (embryo plus endosperm)
wrapped in a hard endocarp (the whole unit, here-
after referred to as the seed). Fruit production fol-
lows a supra-annual cycle of 2 or 3 years, depending
on climatic conditions. Insect pests, especially Dacus
oleae (Diptera), a pulp predator, and Prays oleae
(Lepidoptera), a seed predator, can prevent seed dis-
persal. A number of small bird species also act as
pre-dispersal predators by consuming only the pulp
of the fruits (mainly Fringilla coelebs and Parus
major) or the seed (Carduelis chloris and
Coccothraustes coccothraustes). Small-to medium-
sized frugivorous birds, mainly species of the genera
Turdus and Sylvia, are the dispersal vectors. Seeds
are dormant for around 20 months during which
time they may be consumed by rodents (almost
exclusively Apodemus sylvaticus) and more rarely by
ants (Messor capitatus, M. barbarus and
Aphaenogaster senilis). Epigeal germination occurs
during the second winter after dispersal. The
emerged seedling can be a€ected by water stress,
physical damage (e.g. by trampling and fallen
branches), generalist vertebrate and invertebrate her-
bivores, sap-feeding insects (mainly Euphyllura oli-
vina, Homoptera), and fungal attack.
Approximately 1 year after germination, the seed-
ling acquires adult vegetative traits (woody stems
624 and wax-covered leaves) and becomes a sapling.
Avian-seed Reproductive age is achieved after 7 or 8 years
dispersal and under garden conditions, but much later in the ®eld
seedling (P. Rey, personal observation). The adult plants can
recruitment live for hundreds of years.
The study was conducted in dense scrubland at
Sierra Sur de JaeÂn (37 400 N, 3 450 W; JaeÂn pro-
vince, southern Spain). Between the lowlands and
the mountains of the region, the landscape is typi-
cally made up of a mosaic of large patches of the
scrubland (of a few hectares in area) scattered
among olive orchards, pine forests and old ®elds.
The total scrub cover in the study site is 66.8% and,
of this cover, Pistacia terebinthus accounts for
30.2%, Olea europaea 13.9%, Quercus coccifera
11%, Phillyrea latifolia 5.8% and Rhamnus lycioides
5.2%. Other species, such as Pistacia lentiscus,
Crataegus monogyna and Rosa canina, each account
for less than 1%.
The climate is of the Mediterranean type (ElõÂ as &
Ruiz 1977), with a mean temperature of 16  C and a
mean annual rainfall of 539 mm. During the seaso-
nal drought (June to October, with rainfall dropping
to about 10 mm per month in July and August), the
mean monthly temperature ranges from 23.0  C in
June to 27.4  C in July (SinambA DifusioÂn 1996).
The area su€ered a severe supra-annual drought
from 1991 to late 1995, followed by one rainy year
(745 mm) and two average years.
Olea trees fruited copiously during the 1992±93
and 1993±94 fruiting seasons, having respectively
9999 ‹ 5988 (range 599±20638) and 3237 ‹ 5179
(range 0±28183) fruits per tree. In 1994±95 and
1995±96 the trees hardly produced any seeds, but
again set large crops in 1996±97.
SAMPLING DESIGN
Fig. 1 summarizes the stages, processes and factors
analysed in this study: pre-dispersed seeds are those
contained in a full-sized fruit; dispersed seeds are
the seeds deposited on the ground after consump-
tion by dispersers; seedlings are classed as newly
emerged plants still bearing the cotyledons (we con-

# 2000 British
Ecological Society Fig. 1 Diagram of recruitment to show stages (rectangles), processes (ovals) and factors in¯uencing processes (left hand
Journal of Ecology, side). Values for process-speci®c transition probabilities (TPs) and cumulative probabilities up until that stage (shown in ita-
88, 622±633 lics) are given. Stage-speci®c TPs can be obtained as the product of the process-speci®c TPs involved in each stage.
625 sider a seedling to have emerged when its cotyledons
P. J. Rey & have expanded completely); saplings are classed as
J. M. AlcaÂntara plants that have acquired vegetative adult charac-
ters, generally about 1 year after germination.
The analyses also give information about the spa-
tial dynamics of recruitment. We consider microsites
occupied by di€erent shrub species to represent dif-
ferent microhabitats, and the transition from pre-
dispersed to dispersed seed (representing the prob-
ability of arrival) in each leads to the ®rst spatial
array in the recruitment diagram (Fig. 2). Similarly,
the transitions from dispersed seed to seedling and
from seedling to sapling give rise to new spatial
arrays characterized by the di€ering probability of
emergence (here de®ned as the ratio of density of
emerged seedlings : density of seeds deposited by
birds) and survival, respectively.
Assuming that the processes are independent, the
product of the process-speci®c TPs occurring within
each stage will determine the stage-speci®c TP, and
the product of all TPs will determine the OPR.
Table 1 summarizes the analyses undertaken.
Pre-dispersed seed
Dispersal probability and the proportion of damage
by biotic and abiotic factors were estimated as
described in detail in AlcaÂntara et al. (1997a, b).
Brie¯y, during the 1993±94 fruiting season, we
marked four branches on all the fruiting trees at the
study site (n ˆ 39). We monitored the fruits on each
branch fortnightly and counted the number a€ected
by each of the factors shown in Fig. 1. From these
data, we estimated the number of seeds dispersed as
the number of healthy ripe fruits that had disap-
peared from each branch between censuses. This
number was corrected for fruits abscissed or
dropped by birds, based on fruit counts made in
quadrats placed beneath the branches.

Fig. 2 Diagram of the spatial dynamics of recruitment. Each column depicts recruitment dynamics in a microhabitat de®ned
# 2000 British by the shrub species present. Values shown are process-speci®c transition probabilities (TPs), with overall probabilities of
Ecological Society recruitment given at the base of each column (shown in italics). The width of the box line re¯ects the relative suitability of
Journal of Ecology, each microhabitat for overall recruitment within each stage. A, seed arrival; E, seedling emergence; Ss, seedling survival;
88, 622±633 Sps, sapling survival.
 626

seedling

88, 622±633
Avian-seed

recruitment
dispersal and

# 2000 British
Ecological Society
Journal of Ecology,
Table 1 Summary of the probabilities and sampling procedures used in this study

Probability Acronym Cohort studied Sample unit Weighting variable1 Assessed

Escape from pre-dispersal losses2 PreD 1994/95 Tree Tree/tree crop size Number of healthy fruits
Seed dispersal2 D 1994/95 Tree Tree/tree crop size Number of healthy fruit removed by birds
Seed arrival3 A 1994/95 0.5  0.5 m seedfall quadrats ± Seed density
Escape from post-dispersal predators2 PostD 1996/97 Protected seedfall traps and trays Relative cover of microhabitats Number of dispersed seed predated
Germination2 G 1994/95 open to predators Relative cover of microhabitats Number of seeds germinated
Experimental sowing sites
Seedling emergence3 E 1994/95 2  2 m sampling plots ± Number of seedlings
Seedling survival2,3 Ss 1994/95 2  2 m sampling plots Relative cover of microhabitats Number of plants (seedlings) surviving the ®rst year
Survival of 1-year-old saplings2,3 Sps1 1994/95 2  2 m sampling plots Relative cover of microhabitats Number of plants (saplings) surviving the second year
Survival of 2-year-old saplings2,3 Sps2 1994/95 2  2 m sampling plots Relative cover of microhabitats Number of plants (saplings) surviving the third year
Survival of old-saplings in ®rst year OSps1 Before 1994 4  4 m sampling plots Relative cover of microhabitats Number of old-saplings surviving after 1 year
of study2,3
Survival of old-saplings in third year OSps3 Before 1994 4  4 m sampling plots Relative cover of microhabitats Number of old-saplings surviving after 3 years
of study2,3
Survival of old-saplings in fourth year OSps4 Before 1994 4  4 m sampling plots Relative cover of microhabitats Number of old-saplings surviving after 4 years
of study2,3

1
The weighting variable is the sampling stratum with which each probability was sampled. The relative abundance of each stratum was used to calculate population TPs and OPR. Weighting variables
were not necessary to calculate TPs in the analyses by microhabitat (i.e. the spatial dynamics of recruitment).
2
Probabilities used in the exploration of the overall probability of recruitment.
3
Probabilities used in the exploration of the spatial dynamics of recruitment.
627 This stage can also be in¯uenced by certain char-
P. J. Rey & acteristics of the habitat and individual trees. For
J. M. AlcaÂntara each fruiting tree we measured: crop size, mean
fresh weight of fruit, seed and pulp, mean pulp : seed
ratio, percentage of scrub cover in an area 6 m
around the trunk, and distance to the nearest con-
speci®c reproductive adult.
Dispersed seed
The spatial distribution of seeds after dispersal is
analysed as detailed in AlcaÂntara et al. (2000a).
Brie¯y, in April 1994 (after the fruit removal period)
we sampled seed density around each tree along
four transects placed at right angles to each other.
Within each transect, we counted seed density in 0.5
 0.5 m quadrats located 0, 1, 3, 6, 9 and 12 m away
from the trunk. In each quadrat we noted the micro-
habitat (O. europaea, P. terebinthus, P. lentiscus, Q.
coccifera, R. lycioides, P. latifolia, C. monogyna, R.
canina or open interspaces).
Full details of the monitoring of post-dispersal
seed predation are given in AlcaÂntara et al. (2000b).
Brie¯y, in October 1996 we placed 10 sampling sta-
tions randomly in each of the ®ve most abundant
microhabitats throughout the study site (O. euro-
paea, P. latifolia, P. terebinthus, Q. coccifera and
open interspaces). Each sampling station consisted
of a seed-fall trap (a 26  33  5-cm aluminium pan
protected by a wire mesh to prevent seed removal
by rodents) and an adjacent plastic-net tray (15  15
 3 cm) that was open to predators. We collected
the seeds from each trap fortnightly until October
1997 and moved them into the tray to expose them
to predators. Litter that accumulated in the trays
was not removed so that seeds became naturally hid-
den during the study period. This method yields the
number of fallen seeds at each sampling point (i.e.
collected by the seedfall traps) as well as the number
of seeds predated (i.e. those that had disappeared
from the trays), and thus estimated the probability
of escape from post-dispersal predation.
In December 1994, 2400 seeds collected during
the analysis of the spatial distribution of seeds were
distributed within 66 sowing sites, half under scrub
and half in open sites. Each sowing site was pro-
tected with a cage made of 30  30  10-cm wire
mesh to prevent rodent predation. Before sowing,
we removed all the seeds that were naturally present
in these sites. In subsequent fruiting seasons, we pre-
vented seed arrival by attaching a translucent piece
of cloth to the cage ceiling. The sowing sites were
monitored for germination fortnightly throughout
the period of natural seedling emergence (December
# 2000 British
to May). We considered that germination had
Ecological Society
Journal of Ecology, occurred whenever the endocarp was split and the
88, 622±633 radicle had emerged.
Seedlings and saplings
In December 1994, we chose ®fty-three 2  2-m per-
manent seedling sampling plots; 28 of these plots
were located on four randomly positioned transects
(seven plots per transect, 5 m between plots). To
compensate for the low frequency of some microha-
bitat types in these transects, we randomly chose 10
additional plots under Olea, 10 under Phillyrea and
5 under Quercus. Thus, our sampling design was clo-
ser to a strati®ed random than a strict random
design.
From January 1996, we monitored the number of
seedlings within the plots at monthly intervals.
Seedlings emerging in that year were labelled and
checked monthly for survival until December 1998.
The development of mature characteristics (at which
point they were classi®ed as saplings) and the cause
of mortality if they died were recorded.
To determine the survival probability of older
saplings, we also marked all non-reproductive indi-
viduals already present in 1994 (hereafter called
`old-saplings') within and around the seedling sam-
pling plots. A 4  4 m plot was centred on each seed-
ling plot to obtain a larger sampling unit for plants
in this less abundant stage. We monitored the survi-
val of old-saplings in December 1995, 1997 and
1998.
TRANSITION PROBABILITIES
Transition probabilities (TPs) were calculated as the
ratio of number of individuals completing a stage :
number of individuals entering that stage. This ratio
is used directly when computing TPs within micro-
habitats (i.e. in the exploration of spatial dynamics).
To extrapolate microhabitat information to the
population OPR, it is necessary to weight TP values
by the relative abundance of the sampling stratum
(trees or microhabitats, see Table 1). Interpretation
of some TPs requires consideration of the limita-
tions in our sampling procedures. Our estimate of
escape from post-dispersal predation (PostD) has
two shortcomings. First, this estimate was calculated
for the 1996±97 season, and consequently does not
relate to the cohort monitored for all the other pro-
cesses. The values could lead to under- or over-esti-
mates of the level for the 1994 cohort (see Results)
because inter-annual variation in seed predation by
rodents is common (Schupp 1988, 1990; Ostfeld et al.
1997). Secondly, the period for which seeds were
exposed to predation (11 months) was shorter than
that necessary for germination (around 20 months)
and this could lead to an over-estimated PostD.
Seeds are, however, naturally buried by litter under
®eld conditions and detection by rodents is reduced
(Hulme 1994). For a given microhabitat, A (the
probability of seed arrival) was de®ned as the ratio
of mean seed density in this microhabitat : the sum
628 of mean densities of seeds in all the microhabitats,
Avian-seed and therefore provides a measure of the relative like-
dispersal and lihood of seeds being deposited in each microhabi-
seedling tat. In the absence of germination data from each
recruitment microhabitat, our values for E (the probability of
seedling emergence in a speci®c microhabitat) were
obtained assuming that the seedlings that emerged
in 1996 and 1997 came from those seeds dispersed
during the 1993±94 fruiting season that escaped
post-dispersal predation (note that the trees did not
produce seeds in 1994±95 and 1995±96). Thus, we
calculated E as the ratio of the mean number of
seedlings emerged : the mean number of seeds arriv-
ing in each microhabitat.
STATISTICAL ANALYSES
Parametric statistical analyses (correlations and
ANOVAs) were used. When necessary to meet
assumptions of the tests, data were angular trans-
formed in the case of percentages, or Freeman-
Tukey transformed in the case of density values
(Zar 1984). Non-parametric tests (Spearman rank-
correlation, Kruskal±Wallis analysis of variance and
Kendall concordance test) were used when the
assumptions for parametric tests were not met even
after transformation. Repeated measures ANOVAs
were used to compare the mean percentages of sap-
ling and old-sapling surviving between microhabitats
and years. In these cases, the variable `year' was
considered as the within-subject e€ect, and the vari-
able `microhabitat' as the between-subject e€ect.
Data are reported as means ‹ 1 SE.
Results
STAGEWISE ANALYSIS AND OVERALL
PROBABILITY OF RECRUITMENT
Pre-dispersal stage
On a per tree basis, pre-dispersal seed damage was
high and variable (45.4 ‹ 4.7% of the crop; range
Table 2 Product-moment correlations between the TPs of processes occurring during the pre-dispersal stage (escape from
pre-dispersal losses and dispersal) and factor types, tree characteristics, and habitat features around the trees (n ˆ 38 trees).
** P < 0.01, * P < 0.05, NS ˆ not signi®cant
Variable
Proportion of loss by biotic factors
Proportion of loss by abiotic factors
Crop size
Fruit fresh weight
Seed fresh weight
Pulp fresh weight
# 2000 British Pulp : seed weight ratio
Ecological Society Percentage scrub cover around the tree
Journal of Ecology, Distance to the nearest conspeci®c reproductive tree
88, 622±633
5.6±100%). Abiotic damage to seeds was higher
than biotic damage, but the e€ect was not signi®cant
(27.7 ‹ 4.4%, range 1.6±98.7%, and 17.6 ‹ 2.2%,
range 0±61%, respectively; paired t-test: t ˆ 1.71,
d.f. ˆ 38, P ˆ 0.09). Escape from pre-dispersal losses
was highly correlated with the overall abiotic
damage, but not with biotic damage, or with any
characteristics of the tree and the habitat around it
(Table 2). Although seed dispersal was relatively low
as a percentage of the initial crop size (32.9 ‹ 4.6%;
range 0±87.5%), 60.59 ‹ 6.58% (range 0±100%) of
the fruits that escaped abiotic and biotic damage
were dispersed. Seed dispersal was negatively corre-
lated with abiotic damage and positively correlated
with both fruit and pulp fresh weight (Table 2).
Dispersed seeds
Overall, 63.4 ‹ 15.8% (range 0±100%) of the dis-
persed seeds escaped subsequent predation. This
percentage was not correlated with seed density (rs
ˆ ÿ 0.24, P > 0.05, n ˆ 28). The probability of seed-
ling emergence (E) in the 1994 cohort (weighted
mean density of emerged seedlings : weighted mean
seed density in the seed rain) was 0.3333, giving a
value of PostD for this cohort (E1994/G1994) of
0.8655. This is higher than the value obtained
directly (0.7008) which may be an underestimate,
although it does not change the general pattern of
the results. This value is used in Fig. 1. Average ger-
mination was relatively low (28.7 ‹ 2.7%), and dif-
fered signi®cantly between open interspaces and
areas under scrub (means 16.6 ‹ 2.4% and 40.2 ‹
3.8%, respectively; F1,64 ˆ 28.25, P < 0.01).
Seedlings
In 1996, 1564 seedlings emerged in the sampling
plots, resulting in a mean density of 7.4 ‹ 1.4 seed-
lings mÿ2 (range 0±44). Overall, 10.8 ‹ 2.1% of the
seedlings survived to reach the sapling stage (range
0±50%). We identi®ed the cause of mortality of
Escape from pre-dispersal losses Dispersal
ÿ 0.27 NS ÿ 0.10 NS
ÿ 0.90 ** ÿ 0.57 **
0.18 NS 0.14 NS
0.13 NS 0.35 *
0.12 NS 0.26 NS
0.14 NS 0.38 *
0.04 NS 0.27 NS
0.03 NS 0.21 NS
ÿ 0.13 NS ÿ 0.19 NS
629 90.7% of the seedlings; these were water stress
P. J. Rey & (70%), herbivory (10%), fungal attack (5.8%), other
J. M. AlcaÂntara causes (trampling, physical damage, non-fungal
infections) less than 1% each. Seedling survival did
not depend on seedling density (r ˆ 0.13, P > 0.05,
n ˆ 43 plots) or on the summed proportion of loss
by biotic factors (r ˆ ÿ 0.13, P > 0.05, n ˆ 43), but
was negatively related to the summed proportion of
loss by abiotic factors (r ˆ ÿ 0.41, P < 0.01, n ˆ 43).
Neither abiotic nor biotic factors were correlated
with seedling density (r ˆ ÿ 0.13 and 0.11, respec-
tively, P > 0.05, n ˆ 43 in both cases).
Saplings
Sapling survival was 77.8 ‹ 6.56% (range 0±100%)
in the ®rst year and 77.8 ‹ 7.27% (range 0±100%)
in the second. The initial sapling density was not
correlated with survival (®rst year: r ˆ 0.25, P >
0.05; second year: r ˆ 0.005, P > 0.05; n ˆ 20 in both
cases). The starting density of older saplings was
0.17 ‹ 0.05 saplings mÿ2 (range 0±1.87). For the
129 individuals present, survival was 77.2 ‹ 7.19%
(range 0±100%) after the ®rst year, 86.5 ‹ 5.1%
(range 0±100%) after the third, and 92.3 ‹ 5.12%
(range 0±100%) after the fourth.
Overall probability of recruitment
Process-speci®c and cumulative probabilities of
recruitment are summarized in Fig. 1. A large
decrease in the number of potential recruits occurred
prior to the seedling stage (cumulative TP indicates
that more than 90% of the potential recruits in the
cohort did not survive to reach this stage).
However, the most critical individual stage was the
seedling stage, and seedling survival in the ®rst year
of life was the most critical process during recruit-
ment, as seen from it having the lowest TP value
(0.09). Cumulative TP declined sharply (by an order
of magnitude) during this stage but, after reaching
the sapling stage, the survival probability increased
by almost one order of magnitude (TP ˆ 0.74 and
0.85 for ®rst and second year saplings, respectively).
Table 3 E€ect of microhabitat on seed density, seed predation, density of emerged seedlings, and starting density of old-sap-
lings (mean across microhabitats ‹1 SE). Microhabitats with the same superscript are not signi®cantly di€erent in post hoc
comparisons (Least Signi®cant Di€erence post hoc test)
Olea Phillyrea
Seed density (mÿ2) 37.2 ‹ 2.8a 14.4 ‹ 3.4a
Seed predation (%) 38.5 ‹ 12.9a 14.3 ‹ 8.0a
Emerged seedlings1 (mÿ2) 20.7 ‹ 5.8a 9.4 ‹ 2.6a
# 2000 British Old-saplings (mÿ2) 0.06 ‹ 0.03a 0.30 ‹ 0.11b
Ecological Society
Journal of Ecology, 1 This ®gure is the summed density of seedlings that emerged during 1996 and 1997, which were assumed to come from
88, 622±633 seeds dispersed in 1994 (see Methods).
This high probability tended to continue to increase
slowly as the saplings became older, as shown by
values of 0.84, 0.95 and 0.96 for older saplings in
the ®rst, third and fourth year of the study, respec-
tively.
SPATIAL DYNAMICS OF RECRUITMENT
Recruitment in each microhabitat is summarized in
Fig. 2. The density of seed arrival di€ered signi®-
cantly between microhabitats (Kruskal±Wallis: H(4,
n ˆ 512) ˆ 195.1, P < 0.001; see mean densities in
Table 3). The probability of seed arrival (A) was
maximum under Olea, whereas it was very low in
open interspaces. Intermediate values were recorded
in Quercus, Phillyrea and Pistacia microhabitats. In
contrast, the probability of escape from post-disper-
sal seed predation (PostD) did not di€er signi®cantly
between microhabitats (F3,24 ˆ 1.00, P > 0.05; sites
receiving no seeds were excluded from the analysis).
Mean density of emerged seedlings di€ered signi®-
cantly between microhabitats (F4,46 ˆ 6.64, P <
0.001; see Table 3 for mean values). The probability
of seedling emergence (E) was more than 0.5 under
Phillyrea, Olea and Quercus (Fig. 2), whereas seeds
in open interspaces and under Pistacia had little
probability of producing seedlings. Ss, the probabil-
ity of seedling survival, was generally low (Fig. 2),
but signi®cantly di€erent between microhabitats
(F4,36 ˆ 2.64, P < 0.05). No seedlings survived in
open interspaces, and Ss was extremely low under
conspeci®cs (TP ˆ 0.04). The highest Ss occurred
under Pistacia and Phillyrea (more than four times
higher than under Olea). Mortality of seedlings
caused by abiotic or biotic factors did not di€er sig-
ni®cantly between microhabitats (F4,36 ˆ 1.44 and
1.81, respectively, P > 0.05 in both cases), although
the incidence of water stress did (F4,36 ˆ 3.42, P <
0.05).
The probability of sapling survival (Sps) was
much higher and more homogeneous between
microhabitats, but was lowest under Olea (Fig. 2). A
repeated measures ANOVA (Table 4a) indicated no
signi®cant e€ects of year, microhabitat or their
Quercus Pistacia Open interspaces
15.6 ‹ 3.4a 9.3 ‹ 2.0b 3.4 ‹ 0.8c
52.3 ‹ 15.4a 25.0 ‹ 20.9a ±
8.4 ‹ 2.6a 0.9 ‹ 0.6b 0.2 ‹ 0.1b
0.61 ‹ 0.33b 0.05 ‹ 0.02a 0.01 ‹ 0.01a
630 Table 4 Results of repeated measures ANOVAs on the per-
centage survival of (a) the 1996 sapling cohort and (b) the
Avian-seed
old-saplings. Microhabitat was used as the between-groups
dispersal and factor and year as the within-group factors. Open inter-
seedling spaces were not included in the analyses as no seedlings
recruitment reach the sapling stage P > 0.05 in all cases
F d.f.
(a) 1996 saplings
Microhabitat 1.07 3, 17
Year 0.58 1, 17
Interaction 0.22 3, 17
(b) Old-saplings
Microhabitat 2.67 3, 15
Year 0.58 2, 30
Interaction 1.45 6, 30
interaction on Sps. Initial density of old-saplings dif-
fered signi®cantly between microhabitats (F1,41 ˆ
4.92; P < 0.01; see mean densities in Table 3), and
their survival probability (Osps) followed the same
trend as for saplings (Tables 4b & 5). The lack of a
signi®cant microhabitat  year interaction indicates
that the inter-annual trend in survival was similar
between microhabitats.
The overall probability of recruitment (OPR, Fig.
2) indicates that seeds under Quercus had the highest
probability of reaching the sapling stage, followed
by those under Phillyrea, whereas there was no
recruitment in open interspaces and little under Olea
or Pistacia. There was a clear lack of concordance
across microhabitats in the stage-speci®c transition
probabilities (Kendall Coecient of Concordance ˆ
0.19, P > 0.05, n ˆ 8, d.f. ˆ 3; open interspaces
excluded). Interestingly, the long-term sapling distri-
bution mirrored the net results of the short-term
processes, i.e. the density of the old-saplings was
positively correlated across sampling plots with the
density of 2-year-old saplings from the study cohort
(r ˆ 0.63, n ˆ 48, P < 0.001).
Discussion
Our approach to the analysis of population recruit-
ment dynamics allowed us to determine: (i) the rela-
tive role of biotic and abiotic factors during
recruitment, (ii) the probability of a seed in a ripe
fruit becoming an established plant, (iii) the pro-
cesses and stages involved in the recruitment
dynamics that acted as the most critical limitations
upon recruitment, and (iv) the spatial dynamics of
recruitment.
RELATIVE IMPORTANCE OF BIOTIC AND
ABIOTIC FACTORS DURING RECRUITMENT
DYNAMICS
Abiotic rather than biotic agents are the most
important factors determining recruitment dynamics
in wild olive. The only other study that has analysed
the e€ect of both biotic and abiotic factors simulta-
neously on the probability of escape from pre-dis-
persal damage or mortality in Mediterranean ¯eshy-
fruited plants reported low and similar incidence for
each group of factors (KruÈsi & Debussche 1988).
Studies on bird-dispersed plants have focused on the
incidence of biotic factors, especially insects
(Manzur & Courtney 1984; Jordano 1987, 1989;
Kirschik et al. 1989; Sallabanks & Courtney 1992;
Valburg 1992a,b; Traveset 1993). We found the inci-
dence of insect damage to be in the same range as
for other populations of Olea in southern Spain (6
and 27% in consecutive years, Jordano 1987; 21%,
AlcaÂntara et al. 1997b) as well as for other ¯eshy-
fruited plants in the Mediterranean, such as
Juniperus communis (3 ÿ 33% in di€erent popula-
tions; GarcõÂ a 1998) or Cornus sanguinea (15%,
KruÈsi & Debussche 1988).
Abiotic rather than biotic factors accounted for
the variation between trees in the probability of
seeds avoiding pre-dispersal damage. We also found
a negative relationship between abiotic damage and
seed dispersal, but this was not strong enough to
outweigh the e€ect of dispersers on the number of
potential recruits entering the dispersed-seed stage.
In fact, much undamaged fruit remained on the
trees at the end of the season (21.7 ‹ 4.7%), sug-
gesting that the large crops sated both dispersers
and pests (AlcaÂntara et al. 1997c; see also Jordano
1987 and Herrera et al. 1994 for other
Mediterranean species).

Table 5 Survival probability for old-saplings in each microhabitat in the ®rst, third and fourth year of study. Data are aver-
aged across sampling units

First year Third year Fourth year

Olea 0.6667 ‹ 0.1826 0.5833 ‹ 0.1443 0.7500 ‹ 0.2500

# 2000 British Phillyrea 0.8598 ‹ 0.1232 0.9000 ‹ 0.0724 0.9514 ‹ 0.0374
Ecological Society Quercus 0.8875 ‹ 0.0515 0.9167 ‹ 0.0833 0.9500 ‹ 0.0500
Journal of Ecology, Pistacia 0.7500 ‹ 0.1443 1.0000 ‹ 0.0000 1.0000 ‹ 0.0000
88, 622±633
631 Among the factors leading to post-dispersal
P. J. Rey & damage, only rodents caused substantial seed losses.
J. M. AlcaÂntara Information on Mediterranean ¯eshy-fruited plants
(GarcõÂ a 1998; Herrera 1984; Herrera et al. 1994;
Hulme 1992, 1997 Verdu & Garcõ a-Fayos 1996)
shows variable levels of post-dispersal seed preda-
tion, ranging from 0.4% for Crataegus monogyna to
62.9% for Pistacia lentiscus; our estimate for Olea
(36.6%) falls in the middle of this range.
Almost 40% of the unpredated seeds germinated
in the ®eld. This value is well below the potential
germination capability of Olea europaea under
laboratory conditions (almost 100%; Mitrakos &
Diamantoglou 1984; Voyiatzis 1995). The labora-
tory studies indicated a strong e€ect of temperature
on the release of dormancy, and the clear di€erences
in germination success found between scrub-covered
sites and open interspaces suggest that abiotic
microenvironmental factors may have played a
major role.
Abiotic factors, especially drought, were also the
major cause of low seedling survival. Moreover,
their e€ect may be even more important than esti-
mated here as in other years three cohorts moni-
tored at the same study site showed much lower
recruitment (more than 95% of seedlings of 1995,
1997 and 1998 cohorts died before completing their
®rst year of life; P. J. Rey et al., unpublished data).
Such sensitivity, which has been observed in other
plant species (Andersen 1989; Houle 1994), is com-
mon under the harsh summer conditions of the
Mediterranean climate (Herrera et al. 1994;
Bustamante et al. 1996; GarcõÂ a 1998).
Sapling survival was, however, very high. This
suggests that the gradual acquisition of the adult
traits typical of a drought-tolerant tree
(Angelopoulos et al. 1996; Schwabe & Lionakis
1996) helps the plant to cope with potentially dama-
ging abiotic and biotic factors. Similar trends of
high sapling survival have been found in other spe-
cies (De Steven 1991; Herrera et al. 1994; Houle
1994; but see GarcõÂ a 1998).
CRITICAL STAGES AND PROCESSES IN THE
RECRUITMENT DYNAMICS OF OLEA
The OPR value (0.00557) indicated that less than
0.6% of Olea seeds became 2-year saplings and, if
we further assume that the old-saplings data actually
represent subsequent survival for our main study
cohort, only 0.4% of seeds would survive to become
7-year-old plants. Such a low OPR value can result
either from a succession of processes with relatively
low TP or from a single process with critically low
TP. Dispersal probability (0.5261) was much higher
than the product of the subsequent transition prob-
# 2000 British
abilities (0.0158). Together with the fact that disper-
Ecological Society
Journal of Ecology, sal did not have the lowest transitional value, this
88, 622±633 ®nding suggests that dispersal was not the most cri-
tical process and (in accordance with our prediction)
does not limit recruitment of Olea.
The critical process for recruitment in this species
was seedling survival (Fig. 1). Factors a€ecting this
process are therefore particularly likely to in¯uence
the species' recruitment dynamics. Our results indi-
cate that water stress was the main determinant of
seedling survival, and results for other cohorts in
this population (P. J. Rey et al., unpublished data)
indicate that it may cause nearly 100% mortality in
some years. Recruitment dynamics of Olea therefore
appear to depend on the occurrence at the appropri-
ate point in each recruitment period of climatic con-
ditions (particularly rainfall levels) that permit early
survival of the seedlings. Biotic factors, in particular
avian dispersers, may well a€ect the amount of
recruitment, but their contribution is overwhelmed
by the e€ects of abiotic factors, such as climate
cycles, on the seedling stage.
SPATIAL DYNAMICS OF RECRUITMENT
Our ®eld design tested the hypothesis that the spa-
tial pattern of frugivorous seed dissemination per-
sists throughout subsequent recruitment. We
therefore explored the demographic consequences of
seed dispersal, which are of paramount importance
(Howe 1989; Schupp et al. 1989; Schupp 1993;
Venable & Brown 1993; Herrera et al. 1994) and yet
are poorly understood (Schupp & Fuentes 1995).
The distribution of Olea seeds across microhabi-
tats is concordant with the spatial pattern of seed-
ling emergence. The high positive correlation across
microhabitats between seed rain and initial seedling
density (rs ˆ 0.90, P < 0.05, n ˆ 5) indicates that
variability of post-dispersal seed predation and fail-
ure in germination between microhabitats are not
large enough to counteract the pattern generated by
dispersers. Once the seedling stage is reached, how-
ever, di€erential survival of seedlings between
microhabitats causes a clear di€erence in the relative
suitability of the microhabitats (see also Gill &
Marks 1991; Houle 1992; Herrera et al. 1994). The
most favourable places for seeds became the worst
for seedlings (see Fig. 2), indicating that a seed±seed-
ling con¯ict (Schupp 1995) does occur in our popu-
lation. For example, the microhabitat under Olea
itself showed the highest probability of seed arrival
and also scored high in seedling emergence, but it
was the worst (apart from open interspaces) for
seedling and sapling survival. The opposite occurred
under Pistacia, where the probabilities of seed arri-
val and seedling emergence were lowest and the
probabilities of seedling and sapling survival were
the highest. Such uncoupling between seed and seed-
ling stages is common in recruitment dynamics (De
Steven 1991; Houle 1992, 1994, 1998; Herrera et al.
1994; Horvitz & Schemske 1994; Schupp 1995).
632 The spatial discordance was mainly due to the
Avian-seed marked contrast between the high probability of
dispersal and seed arrival under Olea (47% of the dispersed seeds
seedling reached this microhabitat) and the low probability
recruitment of survival of post-germination stages in those sites.
In contrast, in other microhabitats the spatial pat-
tern generated by dispersers persisted throughout all
the recruitment stages. Probabilities ran in parallel
throughout the recruitment stages under Quercus,
Phillyrea and, apart from a very low probability of
seedling emergence, under Pistacia.
In order to achieve successful recruitment, Olea
seeds must escape the inhibitory in¯uence of estab-
lished conspeci®cs and reach sites where other scrub
species give cover. It is at these sites that facilitation
occurs. This is their regeneration niche (Grubb
1977), or their habitat choice (Bazzaz 1991).
Although widespread seed dispersal seems to be a
fundamental characteristic for this species, many
seeds were nevertheless not dispersed and of those
that were a high percentage were placed under con-
speci®cs. This apparent ineciency of the dispersers
(Schupp 1993), together with the absence of a match
between the spatial patterns of dispersed seed and
either the 1-year-old seedlings or saplings, suggests
that later acting factors rather than dispersal agents
act to shape the spatial dynamics of recruitment in
this species.
Acknowledgements
The authors bene®ted from the involvement of
Alfonso M. SaÂnchez-Lafuente and Francisco Valera
throughout the course of this work. We also wish to
thank AndreÂs Aguilera, Yayo FernaÂndez, Yiyo
Garcõ a, Jose L. Garrido, Antonio Manzaneda and
Jose M. Ramõ rez for their inestimable help during
®eldwork. Two anonymous referees helped us to
considerably improve this manuscript.
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revision accepted 17 January 2000