Spatial Dynamics of Ilex aquifolium Populations Seed Dispersal and Seed Bank:

Understanding the First Steps of Regeneration

Author(s): Sagrario Arrieta and Francisco Suárez
Source: Plant Ecology, Vol. 177, No. 2 (2005), pp. 237-248
Published by: Springer
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Plant Ecology (2005) 177: 237-248 ? Springer 2005
DOI 10.1007/sll258-005-2186-y

Spatial dynamics of Ilex aquifolium populations seed dispersal and seed

bank: understanding the first steps of regeneration

Sagrario Arrieta1'*, and Francisco Su?rez2

Departamento de Medio Ambiente, Universidad Europea de Madrid, 28670 Villaviciosa de Od?n, Madrid, Spain;
2Departamento de Ecolog?a, Facultad de Ciencias, Universidad Aut?noma de Madrid, 28049 Madrid, Spain;
* Author for correspondence (e-mail: msagrario.arrieta@amb.cie.uem.es; phone: 0034912115621;
0034913978004; fax: 0034916168265)

Received 20 May 2003; accepted in revised form 4 July 2004

Key words: Fleshy fruit, Microhabitat, Seed pr?dation, Seed viability, Spatial aggregation

Abstract

The objective of this study was to analyse quantitatively the spatial distribution of holly (Ilex aquifolium L.) seed rain
and seed bank, and to detect the relationships between these consecutive processes. We measured seed dispersal by
birds and fallen fruits, and also density and viability of seed bank in two Ilex populations in central Spain. Analysis was
made distinguishing the following microhabitats: holly woodland, edge of holly woodland, open grassland 10 m and
100 m from the woodland, fleshy fruit shrubs, dry fruit shrubs, and adjacent non-holly woodland. Spatial distribution
of dispersed and in-soil seeds was measured by the clumping index. Seed rain and seed bank under holly woodlands
were significantly higher than in the other microhabitats. Forest edges and fleshy fruit shrubs were the next micro
habitats with the highest seed rain and seed bank density. Interannual and interlocality variations were not significant.
The relative importance of the different dispersal methods varied between microhabitats, with a similar support of bird
dispersed seeds and fallen fruits within the woodland and a greater influence of cattle dispersal in open areas. Seed
spatial aggregation was significant in both dispersed seeds and soil seeds from holly woodlands and the edge of the
forest. Aggregation under shrubs, grasslands and the adjacent forests evidenced a general random distribution of holly
seeds (only in some cases clumping index was significant). Quantitative differences between seed rain and seed bank
are important. Post-dispersal seed pr?dation did not modify seed rain distribution, which was mirrored in the seed bank
pattern. These two phases of holly regeneration had a heavy spatial influence, determined by the landscape structure
and activity of the dispersal agents, that reflects a differential recruitment potential. Comparisons between both
populations suggest that in the southern locality (Robregordo) holly has a weaker capacity to colonize open areas, and
a stronger recruitment limitation due to propagule availability.

Introduction folium, and Retana et al. 1999). Nevertheless, some

The population dynamic analysis of a plant species
must consider a whole range of processes such as
dispersal, germination or seedling emergence and
survival, as well as their relationships. Most of these
processes have been studied independently (seed
dispersal, Sorensen 1981; Herrera 1987, 1995; seed
bank dynamics, Pickett and Mc Donnell 1989;
Thompson et al. 1997, seedling emergence and sur
vival, Kobe et al. 1995, Peterken 1966 for Ilex aqui
studies have analysed the dynamics of these phases in
conjunction to gain better knowledge of their rela
tionships, trade-offs and links. These more integrated
studies show that regeneration can be locally limited
by propagule availability in some cases or by very low
seedling survival in others (Schupp and Fuentes 1995;
Jordano and Herrera 1995; Garc?a-Fayos and Verdu
1998; Rey and Alcantara 2000). It is also clear that
there are several seed-seedling conflicts (sensu Schu
pp, 1995) which suggest a reappraisal of questions

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238
about the evolutionary implications of the process that
did not appear when only one phase from the whole
process was analysed. Linked to this concatenation of
processes, current ecological analyses require the
inclusion of the spatial component, considering either
intermediate (microhabitats) or small spatial scales
(microsites), which potentially show differences in the
seed dispersal, germination and survival, and as a final
result, in a species' establishment and recruitment
(Eriksson and Ehrl?n 1992; Schupp 1995; Kollmann
2000).
The initial questions for a regeneration analysis are:
where are the propagules, how many are there, and
how long are they available for germination? Seed
bank dynamics of woody species are not always well
understood, and little is known about their spatial
quantitative variability and their temporal relationship
with seed rain. Only with a good knowledge of these
initial processes can we understand some of the
regeneration limitations and the potential trends dur
ing the next step of regeneration dynamics, i.e.,
seedling emergence and survival.
In woody fleshy-fruited species, we can consider
that at a mesoscale level (forest stands), spatial seed
deposition is that derived from the behaviour of dis
perses, in terms of permanence rates, patch feeding
selection and general preferences amongst the differ
ent microhabitats in the sense described by Kollmann
(2000). This is relevant to understand certain pro
cesses such as the 'edge effect', linked to greater
diversity of fleshy-fruited species and higher fruit
consumption rates (Thompson and Willson 1978;
Kollmann and Schneider 1999; Arrieta and Su?rez
2001a), 'gap effect', with possible differential dis
persion and regeneration success between closed
canopies and canopy gaps (Hoppes 1988; Nak
ashizuka et al. 1995), and also the nursing effect of
several attractor shrubs (Mc Donnell and Stiles 1983;
Kollmann 1995; Holl et al. 2000). In addition, if the
spatial pattern in post-dispersal seed pr?dation is dif
ferent from seed rain, it may modify the distribution of
seeds, including differences in the propagule distri
bution in the soil.
At a smaller scale level, within each microhabitat,
seeds may have either a random or clumped deposi
tion, that may have consequences at post-dispersal
stages, such as seed pr?dation or seedling competition
and establishment (Hulme 1994; Nakashizuka et al.
1995). These small-scale details are not usually
analysed in woody species, even though they are
crucial to answer the following questions: what levels
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of aggregation remain from one phase (seed rain) to
the next (seed bank)? Is aggregation cumulative in
time or is it progressively smoothed?.
Fleshy-fruited species are very common in Medi
terranean woody communities (Herrera 2001), and the
recruitment dynamics is well documented in some
typical Mediterranean species like Prunus mahaleb L.
(Herrera and Jordano 1981; Jordano and Schupp
2000), Juniperus thurifera L. (Santos and Telleria
1994; Santos et al. 1999), Pistacia lentiscus L. (Gar
c?a-Fayos and Verd? 1998) or Olea europaea L. (Rey
and Alc?ntara 2000).
Holly is a typical understorey species in beech
(Fagus sylvatica L.), oak (Quercus pyrenaica Willd.,
Q. petraea Liebl.) and pine (Pinus sylvestris L.) for
ests. It is also able to create nearly monospecific
woodlands in several ranges in central Spain where
holly is the dominant canopy tree. These small
woodlots are usually found in open grasslands with
different intensities of shrubs invasion. They now
have a high conservation value due to the recent legal
protection of the species and because of their southern
limit distribution situation (Peterken and Lloyd 1967;
Costa et al. 1997).
Based on its fruit type, the species has endozo
ochorous seed dispersal by birds (Peterken and Lloyd
1967; Guiti?n 1984; 1989; Snow and Snow 1988; but
see Ridley 1930; Obeso and Fern?ndez-Calvo 2003
for barochory dispersion). More recently, endozo
ochorous dispersal by herbivorous vertebrates has
been described for holly (Arrieta and Su?rez 2001b).
Its dispersed seeds can be consumed by a wide range
of rodent species (Williams et al. 2000) and holly
post-dispersal seed pr?dation can be influenced by
phenology, pyrene biomass and other seed morpho
logical characteristics (Obeso 1998; Obeso and Fer
n?ndez-Calvo 2003).
Holly seeds usually don't appear in forest soil seed
bank studies, fitting to a life-strategy typical of late
successional plant communities (Thompson 1992).
Nevertheless, it experiences dormant periods of one
year or longer (Peterken and Lloyd 1967), and recent
studies suggest a short-persistence strategy of the
species (Arrieta and Su?rez 2004).
Due to the mosaic landscape structure of holly
woodlots in central Spain, only the combination of a
quantitative analysis of both processes (seed dispersal
vs seed bank) with their spatial dependence analysis,
will provide a thorough basis for answers to questions
such as: Is self-maintenance of holly populations in
side holly woodlands possible? Do dispersal dynam

ics really favour scrub invasion in adjacent grass
lands?
Our premises were:
Seed rain is strongly influenced at a mesoscale level
by differential seed deposition intensity among mi
crohabitats. Seed rain distribution is aggregated at a
small-scale level.
A range of dispersal methods provides a more
efficient colonisation of safe sites, especially outside
the holly stands to escape from parental effects.
Seed bank distribution mainly resembles seed rain
distribution apart from microhabitats affected by post
dispersal seed pr?dation. Aggregation of seeds in the
soil should also be evident, but probably with a lesser
intensity than in seed rain.
Seed rain and seed bank distribution can define
areas with potential recruitment that are limited by
low propagule availability.
Methods
Study areas
Two study areas were selected: Oncala (province of
Soria, Spain, 1450 m a.s.l.; 41? 57' N, 2? 20' W), and
Robregordo (province of Madrid, 1400 m a.s.l.; 41?
10' N, 3? 30' W). Oncala faces north in a region with
healthy Ilex populations (Oria de Rueda 1992). Rob
regordo is 150 km south of Oncala on a SE-facing
slope. Soil characteristics are similar, with neutral to
acidic bedrock in both areas, evolving to humic
cambisols. The areas slightly differ in total annual
rainfall (704 mm in Oncala, 673 mm in Robregordo),
while the period of water stress according to Walter's
climatic diagrams are almost non-existent in Oncala
but cover at least two summer months in Robregordo
(Arrieta 2002).
The woodlands in the study areas are traditional
agroforestal systems, in common fenced ownership
('dehesas'). The study area of Oncala occupies
approximately 120 ha, and Robregordo 145 ha. They
have been traditionally subjected to extensive grazing
(mainly cattle and horses, Iglesias 1999), sporadic
cereal cropping, and periodic non-intensive wood
cutting (Oria de Rueda 1992). As a result of this
management these landscapes have a mosaic structure
with a combination of dense holly woodlots within
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239
grasslands. Land management intensity has now
changed, leading abandonment of crops, lower cattle
density, and strict control of holly woodcutting due to
its legal protection. In recent years, the local Oncala
population has undertaken supervised cuttings of
fruiting branch for the Christmas market (Garcia
2001).
Sampling design
Seed rain and seed bank samples were collected in a
similar spatially stratified design, distinguishing the
following microhabitats: (1) closed holly woodland,
(2) woodland edge, (3) open grassland 10 m from the
woodland, (4) open grassland 100 m from woodland,
(5) fleshy fruit shrubs (mainly Rosaceae) scattered
throughout the open grassland, and (6) adjacent
woodland closest to the holly woodland (Quercus
pyreanica in Oncala and Pinus sylvestris in Robreg
ordo). During the seed bank study, we also obtained
samples under small canopy openings in the holly
woodland. An additional microhabitat, consisting of
locally dominant dry-fruited shrubs, mainly Fabaceae,
was considered in Robregordo, due to their local
abundance.
In these microhabitats we analysed endozoochorous
seed dispersal by birds and barochory for two years in
Oncala (1996 and 1997), and for one year (1997) in
Robregordo. Sampling was focused on the quantifi
cation of differences in seed rain reaching each
microhabitat. The sampling procedure was similar to
Alc?ntara et al. (2000). In each microhabitat we ran
domly defined 20 sampling quadrats (50 x 50 cm, n =
30 for 100 m grassland in Oncala 1996), and con
ducted sampling under winter conditions in December
(only one sample each winter) when holly dispersal is
most intense (Snow and Snow 1988; Guiti?n 1989).
All holly seeds, fruits, and remains of seeds and fruits
found on the ground in each quadrat were collected in
paper bags. Only seeds and fruits with a glossy
appearance were considered as a product of the cur
rent dispersal season, and those with an old appear
ance or not clearly situated on the soil surface were
rejected. Samples were counted in laboratory during
the two weeks following collection. Bare seeds, both
complete and with pr?dation symptoms, were identi
fied as bird-dispersed (Kollmann 1995), but eaten by
rodents in the latter case. Entire fruits and fruit re
mains were assigned to barochory dispersal. Under
estimation of seed rain by our sampling method in
 240
comparison with the traditional seed trap techniques is
probable, but it makes possible to cover a higher
surface of sampling per microhabitat. At the same
time, Alc?ntara et al. (2000) found no significant
differences when comparing the quadrat sampling vs.
the seed traps techniques.
In 1997, we included a spatial analysis in the
sampling design by placing a grid over the sampling
quadrat to obtain two analysis scales: Scale 1 (12.5 x
12.5 cm), and Scale 2, the original 50 x 50 cm quadrat
(Arrieta and Su?rez 1998).
Cattle seed dispersal was also sampled in June
1996, by 10 random quadrats (20 m2) in all the mi
crohabitats, except the adjacent forest, where cattle
were not present. In each quadrat the number and
surface of cattle dung was registered, and a sample of
4 cm diameter was extracted from each dung for seed
counting. The holly entire seeds density in the
excrements was related to total soil surface, and later
referred to 1 m2 surface (see Arrieta and Su?rez 2001b
for more details).
Soil samples (n = 10) were randomly obtained from
each microhabitat in both localities in March 2000 to
represent the post-dispersal season. Experimental soil
sampling in Oncala during the post-germination sea
son (June) yielded similar results (Arrieta 2002).
Samples (10 x 10 cm surface x 5 cm depth) were
stored in paper bags and analysed over the two
months following collection. The soil was crumbled
in laboratory and all holly seeds, fruits, and remains
found in each sample were withdrawn manually.
We took a subsample of 10 seeds from each soil
sample obtained in the closed canopy and open can
opy microhabitats. These were opened to register the
proportion of blank pyrenes (no seed present). The
rest of the non-empty seeds were subject to the tet
razolium viability test (Hartman and Kester 1975;
Moore 1987; Hendry and Grime 1993).
We compared seed viability data from Oncala with
viability of seeds taken from fruits in the same locality
(see Arrieta and Su?rez 2004 for more details).
Data analysis
Variables of seed and fruit density obtained from
dispersal and soil sampling were square root trans
formed (x' = v^ + 3/8); Zar 1996). We applied a
two-way ANO VA with the combination of the fol
lowing independent factors: MICROHABITAT x
LOCALITY (for seed rain and seed bank comparisons
between Oncala and Robregordo), and MICRO
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HABITAT x YEAR (in Oncala, to contrast interannual
and 1996-1997 dispersal variability). Two scenarios
were considered: Scenario A, contrasting densities
between all microhabitats, and Scenario B, excluding
the holly woodland microhabitat. Pr?dation percent
ages were calculated for every single quadrat and
subjected to the same ANOVA analysis. A post-hoc
LSD test for multiple comparisons was applied when
necessary. The Student test was used to contrast seed
density between fleshy- and dry-fruit shrubs in Rob
regordo, and viability percentages between Oncala
seeds (tree vs. soil). All the percentage data were
previously arcsin transformed (Zar 1996). The
STATISTICA software package (StatSoft 1984) was
used for the statistical analysis.
In order to compare the relative importance of the
different dispersal methods, we analysed data from
bird dispersal and barochory with those showing
endozoochorous cattle dispersal. Seed rain achieved
by barochory was calculated by multiplication of the
fruit's density by the mean number of pyrenes per fruit
(3.34 in Oncala and 3.54 in Robregordo, Arrieta and
Su?rez 2003). We also graphically compared dispersal
data with soil seed density, and calculated an estimate
of the minimum number of years necessary to reach
the observed seed bank densities.
Spatial aggregation of dispersed and soil seeds was
estimated by calculating the Clumping index Ic= (var/
mean ) ? 1. This index, divided by its standard error
(s.e. = ^f{2/(n ? 1)) can be compared with the crit
ical value of Student's t distribution with n-1 d.f.
(Elliot 1983). We contrasted clumping of dispersed
and soil bank seeds by comparing the aggregation
values obtained from dispersal data for Scale 1 (12.5x
12.5 cm) with those from seed bank data (10 x 10 cm)
for the holly woodland microhabitat. The Clumping
index was standardised for this comparison, dividing
in each case this value by its theoretical maximum,
i.e., Ex-1. The index was thus homogenised into the
interval (0-1) to provide a better relative comparison.
Results
Seed rain
ird dispersed seed density within the holly woodland was
between one and two orders of magnitude higher than in
the other microhabitats (ANOVA, Table 1, Table 2, LSD
test, p < 0.05). Outside the woodland, the forest edge and
the fleshy fruit shrubs received a significantly higher
bird-dispersed seed rain (ANOVA, scenario B, Table 2;
 241

Table 1. Mean (+STD) density (1 m2) of complete (CO) and eaten (EA) seeds found in bird-mediated (BI) seed dispersal, and fallen fruits (FR)
and remains of fallen fruits (RE) in the barochorous (BA) seed dispersal sampling. Oncala data shown for both sampling years, 1996 and 1997.
n = 20 samples for each microhabitat. Acronyms of microhabitats are CHW: closed holly woodland, E: edge, G10: grassland 10 m, G100:
grassland 100m, FFS: fleshy fruit shrubs, DFS: dry fruit shrubs, and AW: adjacent woodland. Gaps in Table are non-sampled microhabitats.

CHW E G 10 G 100 FFS DFS AW

ONCALA BI CO 96 157?245.1 4.4?8.7 1.4?2.4 1.6?4.0 4.8?5.9

CO 97 114.6=1=291.5 8.6=1=18.4 1.2?2.9 1.0=1=1.8 2.8?4.1 0.2?0.9
EA96 130.2 ?261.4 2.0?4.0 0.2?0.9 0.0 10.0=1=31.3
EA97 65.4? 120.4 6.2 ?14.1 0.0?0.0 0.0 8.8=? 16.4 0.6?2.0
BA FR96 38.4 ?66.4 0.2 ?0.9
FR97 16.4 ?29.0 0.2 ?0.9
RE 96 22.0 ?46.9 0.4 ?1.8
RE 97 16.6 ?24.9 0.0 ?0.0
ROBREGORDO BI CO 97 84.2 ?143.0 5.4 ?14.4 0.6 ?1.5 0.0 0.8 ?1.6 0.2 ?0.9 0.4 ?1.2
EA97 27.8?46.9 6.8?17.1 0.2?0.9 0.0 0.4?1.2 0.0 0.0
BA FR97 6.4 ?11.3 0.0 ?0.0
RE 97 2.6 ?6.0 0.2 ?0.9

LSD test, p < 0.05). Neither interannual variability nor
differences between localities were significant. Only in
scenario B (excluding holly woodland) were there dif
ferences in seed dispersal densities between localities
(higher in Oncala, see Table 2, analysis B2).
Seed rain under shrubs with dry fruits from Rob
regordo differed not from that under fleshy-fruited
shrubs in the same area (t = 1.44 for total seeds, and t =
1.59 for complete seeds, p > 0.05 in both cases), al
though bird seed rain in the former microhabitat was
also similar to that found in grassland (t = 1.16 for total
seeds, and t = 1.04 for complete seeds; p > 0.05 in both
cases).
Fruit fall was most frequent within the holly wood
land, while at the edge, very few seeds arrive via ba
rochory (Table 1). Barochory intensity was neither
different between localities (t = 1.39; p = 0.18) nor
between years in Oncala (t = 1.40; p = 0.17).
The relative contribution of three sources of seed
rain (endozoochory by birds, endozoochory by cattle
and barochory) differed between microhabitats (Fig
ure 1). In holly woodland the proportions of bird
dispersal and barochory were similar (accounting for
94% of total seed rain). Cattle dispersal was the major
dispersal vector at the edge of the woodland (almost
three quarters of all seeds). Finally, in the grasslands,
there was a similar amount of seeds arriving via bird
or cattle excrements, with no differences related to
distance from the forest.
Post-dispersal seed pr?dation
Pr?dation rates differed between microhabitats (Figure
2), and between localities (higher in Oncala), but not
between years (31% and 32% of pr?dation rate for
1996 and 1997 in Oncala, and 25 % eaten in Rob
regordo, Table 2). We found an interesting significant
interaction between microhabitat and locality (Table
2). This interaction is probably due to a higher pr?
dation intensity outside the holly woodland in Oncala
(specially shrubs and adjacent woodland) and the
main concentration of pr?dation at the edge of the
woodland in Robregordo.
Analysing only complete dispersed seeds (= total -
eaten), as an index of net propagule incorporation,
seed rain distribution did not differ from that found
with total seeds analysis (Table 2).
Seed bank
Total seed density in the soil differed between mi
crohabitats and between localities (2-way ANOVA,
locality: df = 1/126, F = 6.20, p = 0.01; microhabitat:
df = 6/126, F = 34.20, p < 0.01; locality x micro
habitat: df = 6/126, F = 1.47, p = 0.19, Table 3). More
seeds were found inside the holly woodland, both
closed canopy and gaps, and on the edge (LSD test,
p< 0.05). Although seed density at the soil under
fleshy-fruited shrubs was at least 4 to 6 times higher
than in the grassland, no significant differences were
found.
We found a range between 1 to 150 years for the
minimum number of years necessary to reach those
seed bank densities with the measured seed rain
(Figure 3). In Oncala, seed bank formation in holly
woodland would require 15 years, 20 years on the
edge, 12 in grassland (both 10 and 100 m from the

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242

O O O O O O 100%

d?
80% 4
co o O m ^t CN

60%
3 ^
O
^ ^ n- Tj- -* rj 40%

o o ?
o
Q o\
CNrn
r 20% 4
V V

m on r- r
O a
o CHW E GIO GlOO
i? o U
m ?< <?i oow^o^^oo
B ^ Microhabitat
-I -
-5 "o
O 43 o o
-_: On ^ ?: oo M Birds D Cattle Barochory
? CN CN ? ^h on
T3 V rS o V ? o
Figure 1. Relative proportion of seed arrivals in Oncala by three
oo i^ r dispersal methods: endozoochorous bird dispersal, endozoochorous
?3 (X o -H T
un <-? <?? r^ *-<? 0\ ? *-h On m t-h cattle dispersal, and barochory, to the following microhabitats:

II
CHW: closed holly woodland (total seed arrival, 341.0 seeds m-2),
E: edge (20.3 seeds m~2), G10: grassland 10 m far (2.5 seeds m~2)
???OOOOOOCNCNCN???
???CNCNCN'O^DVOOnOnON and G100: grassland 100 m far (3.4 seeds m-2).

43 --H ^ .^H Tf m >/-> co ^ m "?T -?< tj

o ?o

si O
woodland), 47 under fleshy-fruited shrubs, and 150
years in the adjacent woodland. Differences were
1/1 ~ greater in Robregordo: 37 years for the woodland seed
o? -C
2
*C t? 43 X) X) X> bank formation, 63 years for the edge, 125 for fleshy
43 43 -? .J3 43 4343-^43
00^300 00^30 fruit shrubs, 150 for dry fruited shrubs, and 25 years
O 09
for adjacent woodland. In grassland 10 m away we
0> ? ? ^ "s s j s 'a ?%%2 found no seeds in the soil bank, but dispersed seeds
existed (0.6 seeds m~2), so we estimated a period of
one year for seed bank formation in this microhabitat.
We have no data for this estimate in grassland 100 m
away in the southern locality, since both seed bank
2 sa and seed rain were equal to zero.
<U Cu
o
& v?
Spatial aggregation of seeds
?
o O
<: H In both localities, aggregation patterns of bird-dis
>o 'S
s o O
2 persed seeds were similar, especially within and on
31 H
< >
H
< the edge of the holly woodland (Table 4) where seed
2 H-l 2 clumping was very high. Outside the woodland
< <
ID >
(grassland and shrubs), and in the adjacent woodland
< < a random distribution was found in dispersed seeds,
z z
o o except in grassland 10 m away, significantly aggre
5
w
W
H 5 gated in Oncala.
CN Fallen fruits within the holly woodland were also
aggregated, particularly at the larger scale. Soil seed
aggregation was high in the microhabitats with high
seed bank density, i.e., within the holly woodland

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 243
?-h CN Tj
Oncala no ^ t^ ?i
W-) Tj- 00 CN
i/-> no NO

00 Tj- *-< Tf
-H -H -H -H 41 -H -H -H -H 41 41 41
3T ???????????????
CNOOCNCN no */-? io xj- ^o m ~ <?*
oo rt ?- m ^

I
S
o
a
S

55
n 41 -H 41 41 41
?????????????
m '-i On Tf
CHW FFS DFS G10 G100 AW
Microhabitat
4 oo ? On m
CO NO
4 "^-?^-.ooONCNr-??^ oo oo -n
Tj-(NTiTr\o^ND>n^(N - * tj- m
Robregordo 414I-H441414I4I4141 4I4I-H
???????????????
140 o r-r^ONcnTj-oom?ooTi- ? co ^
h oo w ?? o on m *-<
H ?n CN Tj
120
100
80

Ll?
60 ON ?<
Tf ON OO on no
40 OO On m
ON Tj- ^H
SO CN
Tf -^
41 41 41 4 41
20 1 ? ? ? ????????????
m ^?i in no n
CN
0
CHW E FFS DFS G10 G100 AW t-~ On s?
? * CN CN
00 rf m t m
Microhabitat rN -^ no ?! no
41 -H 41 41 41
???????????????
?? On CN OO CN
Figure 2. Mean + STD of percentages of eaten bird-dispersed seeds CN

in 1996 (white bars) and 1997 (black bars), in the different micro
habitats of the two localities. CHW: closed holly woodland, E: edge,
FFS: fleshy fruit shrubs, DFS: dry fruit shrubs, G10: grassland 10
m, G100: grassland 100m, and AW: adjacent woodland. Numbers o<no^ O r^r^^ v?
over bars express the number of samples (from total n = 20) used for NOr^*oooON<Nr^?r>ONNO oo oo -h
m ? c-iTj-No?- 'Otj-oncn ? Tj-m
the mean (those with at least one seed present). -H-H44I414I4I414141 4-H-H
???????????????
ooNOTfmTfoom^i-Tj-Tj- o co *?<
m rf m '?< t^ on m -h

(both closed canopy and gaps), and also at the forest

edge in Oncala. Clumping under fleshy-fruited shrubs
in Robregordo was important in comparison with dry
fruited shrubs. Random distributions predominated in
the seed bank of the open grasslands and adjacent 4
? ?????????????
forests. O
Differences between standardised indices of
clumping for seed rain and seed bank, from data on
the closed holly woodland microhabitat revealed a
higher seed bank aggregation in Oncala, and the in
verse in Robregordo (Table 5).

Seed viability o
o
<
u en
Viability percentages were similar in seeds found in z
o
the soil under both closed canopy and gaps for both

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All use subject to http://about.jstor.org/terms
244

IUUU
1989) or predators. Besides, barochory is almost as
CHW
important as seed dispersal in this microhabitat. The
average number of seeds in holly woodland soil was
100 CHWa
over 5000 seeds m~2 in Oncala, and 4000 seeds m~2 in
CO
a
Robregordo. Reductions in seed bank density in the
CD
CD
E woodland gaps may result from a reduction in ba
^ 10 rochory. These results concur with other studies that
G100 E? found no higher seed rain levels in forest gaps
FFS
CD G10 (Nakashizuka et al. 1995).
CO
a FFS Outside the forest, differences between microhabi
AW* tats are related to dispersal agents and vegetation
AW* DFS structure. The forest edge receives the highest amount
n 1
of seeds from these 'outside' habitats, mainly through
1 10 100 1000 10000
cattle dispersal. Bird dispersal in this microhabitat
Seed bank (seeds m~2) seems to be less predominant than in other forest edge
studies (Hoppes 1988; Fuentes 1991; Murcia 1995),
Oncala ? Robregordo
probably because in our case there is a large fruit
Figure 3. Seed bank and seed rain (bird dispersed 4 cattle dis supply inside the forest.
persed 4 seeds in fallen fruits) relationships in a logarithmic scale. Open grassland is the habitat with the least seed
CHW: closed holly woodland, E: edge, G10: grassland 10 m, G100: rain, regardless of distance from the woodland, and
grassland 100m, FFS: fleshy fruit shrubs, DFS: dry fruit shrubs, and
also has a very small or null presence of seeds in the
AW: adjacent woodland. (Data for G10 and G100 in Robregordo
not shown because seed bank = 0).
soil. This can be related with the general avoidance of
open spaces by Mediterranean frugivorous birds
(Herrera and Jordano 1981; Alc?ntara et al. 2000),
localities (t = 0.9, p = 0.38, df = 17 in Oncala; which leads to rather poor seed dispersal by birds to
t = -1.69, p = 0.11, df = 16 in Robregordo). Mean this microhabitat, being herbivorous vertebrates the
viability of non-empty pyrenes in Oncala was 80.4 ? fundamental dispersal agents in these open areas
17.2%, while in Robregordo, 65.0 ? 22.4% (t = 1.77, (Schupp et al. 1999; Arrieta and Su?rez 2001b).
p = 0.08, df = 35). Compared to seeds collected from Fleshy-fruited shrubs receive more seeds than open
fruits in Oncala (27.2% empty pyrenes, and 68.5 ? areas. This is also a reflection of post-feeding patch
16.5% of the rest with a viable embryo, Arrieta and selection by birds, well described in several scrubland
Su?rez 2004) we found no significant differences in systems (Mc Donnell and Stiles 1983; Schupp and
total viable seed proportions in this locality Fuentes 1995; Duncan and Chapman 1999; Slocum
(t = -1.88, p = 0.08, df= 31). 2001; Holl 2002). This enforces the patchy distribu
tion generally found in animal-dispersed species
(Harper 1977; Kollmann 2000), and could indicate a
Discussion secondary succession process in which holly and
other fleshy-fruited species benefit from scrub devel
Holly seed rain opment (Kollmann 1995; Arrieta and Su?rez 2001a).
The lower intensity of seed concentration under
A similar pattern of seed deposition was found in both shrubs in Robregordo may be due to the dominance of
localities, i.e., intense seed rain in holly woodlands Rosa species, a less palatable genus for birds (Snow
combined with relatively little seed rain outside them. and Snow 1988) in comparison with Crataegus,
This distribution was mirrored by variation in seed Viburnum, Ligustrum, and Lonicera, which are fairly
bank densities. abundant in Oncala. This low attraction of Rosa
Higher seed density in closed forests and beneath shrubs may also explain the absence of differences
parental trees is well documented (Jordano and Her with seed rain under dry-fruited shrubs in Robreg
rera 1995; Houle 1995; Obeso and Fern?ndez-Calvo ordo, as also found in other Mediterranean systems
2003), mainly due to a great visit rate of birds because (Alc?ntara et al. 2000). Rather than a strong difference
of higher fruit concentration, and for sheltering of between fleshy- and dry-fruited shrubs in relation to
weather inclemency (Castroviejo 1975; Guiti?n 1984; perching by birds, there may be an attraction gradient

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 245

Table 4. Clumping index for complete dispersed seeds ('seed rain'), fallen fruits (only under holly woodland), and seed bank in Oncala and
Robregordo. Data for seed rain and fallen fruits given in the two sampled scales from year 1997. Data for seed bank given for sampling scale
10x10 cm. (?), impossible to calculate index, due to seed density equal to zero in that scale. (*), significant aggregated distribution. Acronyms
of microhabitats are CHW: closed holly woodland, HWG: holly woodland gaps, E: edge, G10: grassland 10 m, G100: grassland 100m, FFS:
fleshy fruit shrubs, DFS: dry fruit shrubs, and AW: adjacent woodland.

CHW E G10 G10 FFS DFS AW

Bird dispersed Fallen fruits

Oncala SEED RAIN Scl 11.5* 0.2* 0.4 - 0.0 -0.1 not sampled 0.0
Sc2 184.3* 11.8* 9.0* 0.8* -0.2 0.5 0.0
SOIL BANK 37.8* (CHW) 5.7** -0.2 0.2 -0.2 not sampled 0.5
14.2* (HWG)
Robregordo SEED RAIN Scl 2.9* 1.0* -
Sc2 59.7* 4.0* 8.5* -0.1 - -0.2 0.0 -0.1
SOIL BANK 62.0* (CHW) 1.1 - - 2.6* -0.2 0.0
9.3* (HWG)

Table 5. Standardised dumping Index in closed holly woodlands been misclassified as having a transient seed bank
for both localities. '>' and '<' refer to aggregation intensity.
(Kollmann 2000).
Seed bank (S.B.) Seed rain (S.R.) Diagnosis
Oncala 0.073 0.338 S.B. < S.R.
Robregordo 0.155 0.088 S.B. > S.R. Seed pr?dation

Seed pr?dation proportions must be considered as

based on the interaction of both species-specific dif
ferences and structural characteristics (Slocum 2001;
Robinson and Handel 1993; Mc Donnell 1986).
Adjacent non-holly forests receive little holly seed
rain. Although distance can influence woodlots colo
nization (Hewitt and Kellman 2002), this is probably
not a limiting factor in this case. Birds that mainly
visit these forests are probably only occasionally holly
dispersers such as Columba palumbus, Erithacus
rubecula, Sylvia atricapilla, while 'true' dispersers
(those that mobilise a higher quantity of Ilex seeds),
primarily thrushes (Turdus spp.), display territorial
behaviour including holly tree defence (Snow and
Snow 1988). Holly colonization of these forests ap
pears possible but slowed down, with possible limi
tations on propagule availability, as seen in the seed
bank analysis. These forests are better matched to the
more commonly sampled mature temperate forests,
where holly seeds are much less abundant. This low
density, united to the seed dormancy (Arrieta and
Su?rez 2004), may be the reason why I. aquifolium
has been regarded as a species with no permanent
seed banks, specially when seed bank studies are
undertook by germinating seeds protocols, that can
bias persistence estimates in species that experience a
kind of dormancy (Thompson et al. 2003). Other
fleshy fruit taxa like Rosa and Crataegus have also
conservative estimates due to the estimation method,
while higher pr?dation percentages have been found
for this species (Williams et al. 2000; Obeso and
Fern?ndez-Calvo 2003). The increase of pr?dation
rates with seed rain density and forest or shrub cover
presence is probably due to rodent habitat preferences
(Price and Jenkins 1986; Hulme 1994, 1996; Koll
mann 1995; 2000; Hulme and Hunt 1999; Kollmann
and Buschor 2002).
How important is seed pr?dation for recruitment
in this species? In plant populations of species with
a kind of persistence of seeds and microsite
dependent regeneration (both processes occurring in
holly, Arrieta and Su?rez 2001a; 2004), seed pr?
dation usually has a limited effect on plant popu
lations (Hulme 1996; Kollmann et al. 1998). In the
inside of the holly woodland the high densities of
seeds in the soil indicate a low influence of pr?
dation in recruitment. In the edge and shrubs mi
crohabitats, where some seeds were eaten, a
considerable seedling emergence occurs (Arrieta and
Su?rez 2001a), so we cannot assert that pr?dation is
limiting recruitment. Only at the oak woodland in
Oncala we find that the concurrence of low seed
rain, and high seed pr?dation may contribute to the
observed low seedling emergence (Arrieta and
Su?rez 2001a).

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246
Seed rain - seed bank dynamics
Seed bank density was on average 10-20 times higher
than seed rain. Recent studies reveal that 80% of seeds
germinate or lose their viability in the first three years,
suggesting a short-time persistence of 1 or more years
(Arrieta and Su?rez 2004). This fact does not support
the 10 to 20 years accumulation period that would be
necessary to explain the observed seed bank densities.
These quantitative differences may be explained by
assuming that either the dispersal sampling year was
poor in dispersal, or that the seed bank sampling year
was extremely good in seed rain. In both cases, the
existence of some masting dynamic should be ac
cepted, as reflected in seed bank but not detected in
our one- or two- year seed rain samplings.
Spatial aggregation of seeds
Analysing the possible origin of the patchy seed dis
tribution at a small scale, we can consider the smallest
level of aggregation due to the frugivorous dispersal,
that is the within excrement clumping: Guiti?n (1989)
detected a mean of 2.5 holly seeds per excrement of
Turdus iliacus. This is the only aggregation level that
can occur in every microhabitat, including those with
a low seed density. On the ground of holly woodlands
there are other clumping processes, not only for seeds
but also for fallen fruits: accumulation due to micro
topography or seed and fruit concentration under fe
male trees. Our sampling scales should detect the
patch size originated by microdepressions, but a patch
size larger than 50 x 50 cm may exists.
Seed rain accumulation from different years can
diminish aggregation intensity at the smaller spatial
scales and increase aggregation at larger scales (i.e.,
under female trees or between closed canopies and
canopy gaps). If this occurs, higher aggregation values
should be found in seed rain (Scale 1) than in the seed
bank, as is the observed under holly woodland in
Oncala. If the results in Robregordo are not consistent
with those of Oncala, it is probably as a result of the
smaller seed rain density found in the southern
locality.
In conclusion, we found that spatial distribution of
seed rain and seed banks can be explained as a
function of the mosaic landscape structure and the
dispersal agents. A similar pattern of propagule
availability among microhabitats can be identified in
both localities, which in some cases limits the
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recruitment potential. The generalised lower level of
seed rain and seed viability in the Robregordo popu
lation, plus their heavier concentration under stands of
trees (less efficiently colonizing of the outside areas),
could together be indicative of a weaker capacity for
sexual regeneration in this southern locality. Any fu
ture study that focuses on seedling emergence and
survival, or even forest management of these wood
lands, should take into consideration these natural
functions of propagule distribution.
Acknowledgements
This research was supported by a PhD research grant
from the Regional Education Department, Comunidad
de Madrid. The Regional Government Environment
Departments for Madrid (Consejer?a de Medio Am
biente) and Soria (Direcci?n Territorial de Medio
Ambiente y Ordenaci?n del Territorio) granted per
mits for the field work. Prof. Eugene Schupp, and two
anonymous referees gave us very interesting com
ments to the final improvement of this work.
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