Composition, size and dynamics of the seed bank in a mediterranean shrubland of Chile

Austral Ecology

(2004)

29

, 574–584

Composition, size and dynamics of the seed bank in a mediterranean shrubland of Chile

JAVIER A. FIGUEROA,

1

* SEBASTIÁN TEILLIER

2

AND FABIAN M. JAKSIC

1

1

Center for Advanced Studies in Ecology & Biodiversity, Pontificia Universidad Católica de Chile, Casilla 114-D, Santiago CP 6513677, Chile (Email: [email protected]) and

2

Escuela de Ecología y Paisajismo, Universidad Central de Chile, Santiago, Chile

Abstract

Analysis was performed of the richness and abundance of woody species, forbs, and annual grasses inthe easily germinating soil seed bank (henceforth seed bank) in a mediterranean shrubland of central Chile. Theeffects of successional development after fire and by microsite type (underneath or outside shrubs) on the densityof seeds in the soil, and the relationship of species abundance in the seed bank with its abundance in the above-ground vegetation was examined. A total of 64 plant species were recorded in the seed bank, of which 44 were annualor biannual. Eight species were woody and another eight were perennial herbs. Four could not be identified to specieslevel. The highest richness of established herbaceous species was recorded in late spring, with 31 species. Theregeneration of the herbaceous vegetation was driven by the annual production of seeds and by a reserve of short-lived propagules in the soil. Density of all germinating seeds was significantly higher during late spring and latesummer. Density of grass seeds was greater during late spring, while that of all other species was greater during latesummer. Annual grass seeds accumulated in higher proportion at exposed microsites rather than under woodycanopy, and in young (< 5 years old) and intermediate-age patches (10–20 years old) rather than in maturevegetation (30–50 years old). The abundance of established woody and herb species was uncorrelated with that ofthe seed bank.

Key words:

central Chile, matorral, seed-bank germination, seed burial, soil-seed dynamics, transient seed-bank.

INTRODUCTION

Seed banks are important for the structure, dynamics,and spatiotemporal distribution of mediterraneancommunities of plants (Parker

et al

. 1989; Ortega

et al

. 1997; Peco

et al

. 1998). Indeed, variation in seedbank dynamics is often reflected in the composition,distribution and dominance of above-ground species(Parker & Kelly 1989). However, a direct relationshipbetween above-ground vegetation and seed bank doesnot always occur (Thompson 1986; Leck 1989; Parker& Kelly 1989; Rice 1989), in part because some plantsalternate seed and vegetative reproduction. Further, thedominance of annual and short-lived perennial herbs inthe above-ground vegetation influences the temporaldynamics of the seed bank in mediterranean grasslands(Major & Pyott 1966; Leck 1989; Rice 1989; Ortega

et al

. 1997; Holmes 2002), where seed density fluctu-ates between a maximum in summer and a minimumin spring (Rice 1989; Levassor

et al

. 1990; Russi

et al

.1992a; Olivares

et al

. 1994).Distribution patterns of seeds in the soil may be

affected by microsites available beneath or outside thecanopy of woody plants (Kemp 1989; Zammit &

Zedler 1994; Bertiller 1998; Pugnaire & Lázaro 2000).Soil beneath shrubs accumulates biomass, receiveslower light intensity, has greater humidity, and issubjected to moderate temperatures in comparison toexposed microsites away from the canopy (Del Pozo

et al

. 1989; Bertiller 1998). Thus, microsites may affectplant establishment and hence the seed bank (Bertiller1998). On the other hand, seed banks respond toenvironmental disturbances (Parker & Kelly 1989;Levassor

et al

. 1990) and stages following the distur-bances (D’Angela

et al

. 1988; Levassor

et al

. 1990).Specifically, seedling density after fire is particularlyvariable in mediterranean regions, because of speciescharacteristics and seed bank persistency (Keeley &Nitzberg 1984; Parker & Kelly 1989). The Chileanmatorral consists of a mosaic of patches differing incomposition of woody plants and in successional stagesafter fires (Keeley & Johnson 1977; Fuentes

et al

. 1983;Armesto & Pickett 1985; Fuentes

et al

. 1986; Muñoz &Fuentes 1989; Armesto

et al

. 1994; Holmgren

et al

.2000). This heterogeneity is important for plantsbecause patches modify local microenvironment andresource availability, and hence seed density anddistribution (Bertiller 1998).

Factors contributing to the distribution and dyn-amics of the herbaceous seed bank are little known inthe Chilean matorral (Jaksic 2001a). However, the seed

*Corresponding author.Accepted for publication February 2004.

SEED BANK IN THE CHILEAN MATORRAL 575

bank of woody species is reportedly small, with analmost complete absence of some of the major elementsof the vegetation in the seed bank (Fuentes

et al

. 1984;Jiménez & Armesto 1992). Here we (i) compare rich-ness, abundance and persistence of seeds of woody,herb and annual grass species in the seed bank; (ii)determine if successional stage after fire, presence orabsence of canopy of woody species, and season of theyear, affect the seed bank; and (iii) determine if thespecies abundance in the seed bank is correlated withthat of above-ground vegetation. We report that theherb seed bank in the matorral is highly dynamic andtransient, showing as much spatio-temporal variabilityas in other Mediterranean regions (Parker & Kelly1989; Russi

et al

. 1992a; Peco

et al

. 1998). This may bedue to the annual life cycle of the dominant species inthe herbaceous layer (Montenegro

et al

. 1991; Arroyo

et al

. 1995), and to heterogeneity imposed by firedisturbances (Fuentes

et al

. 1986; Jaksic 2001b).

METHODS

Study site

The locality of San Carlos de Apoquindo (33

�

27

�

S,70

�

42

�

W) is located in the foothills of the AndeanRanges at 1000 m elevation and about 20 km east ofSantiago (Fig. 1). It has a mediterranean-type climate,with a summer drought (6–7 months long) and aperiod of winter precipitation (May to September).Mean annual precipitation is 376 mm, falling mostly asrain, with sporadic snowfall. Mean annual temperatureis about 16

�

C. Mean minimum temperature is 10

�

C,while mean maximum temperature is 23

�

C. Soil isderived from volcanic rock. The upper most soilstratum consists of a thin layer of fine clayish sand.

In the last four centuries, central Chile hasexperienced disturbances due to changes in land use,herbivore browsing, and fires of human origin (Fuentes1990; Aronson

et al

. 1998). Currently, vegetation con-sists of sclerophyllous evergreen shrubs, and a herblayer dominated by annual species (Gulmon 1977;Keeley & Johnson 1977; Fuentes

et al

. 1983; Groves1986; Montenegro

et al

. 1991). The shrubland isdominated by the woody species

Lithrea caustica

,

Quillaja saponaria

,

Baccharis

spp. and

Colliguajaodorifera

, while the herb layer is dominated by theannuals

Bromus berterianus

,

Vulpia bromoides

and

Erodium cicutarium

, as well as by perennial species ofthe genera

Conyza

and

Gamochaeta

. The main periodof flowering and fruiting of the flora in central Chileis during spring and summer (Arroyo

et al

. 1981;Hoffmann

et al

. 1998; Jaksic 2001a).

Above-ground vegetation

Herbaceous plants were sampled during winter 2001,and in winter 2002, while woody plants were sampledduring winter 2001. At the beginning of the study, weselected two replicates for each of the three mostfrequent successional stages arising from fire (Table 1).

Fig. 1.

Location of the study site at San Carlos deApoquindo, central Chile.

Table 1.

Identification of succesional stage after fire selected in the study site and characteristics of the vegetation sample

CharacteristicsSuccessional stage

Young Intermediate Mature

Dominant woody species

Baccharis

spp.

Colliguaja integerrima Quillaja saponariaSolanum ligustrinum Lithrea caustica Lithrea caustica

Years after fire < 5 10–20 30–50Canopy height (m) < 1.5 1.5–3.0 5.0–15.0Cover of woody canopy (%) < 30 30–70 > 70No. of replicates 2 2 2Vegetation transects 6 6 6Soil samples 60 60 60

576 J . A. FIGUEROA

ET AL.

The successional stages were selected according toArmesto and Pickett (1985) and dates of fire wereobtained from local people (pers. comm., 2001), andshould be considered as approximate. The replicateswere at least 2 km apart. In each replicate wherevegetation data and soil samples were obtained in25 m

�

25 m plots, and where domestic herbivores(horses) were excluded.

Abundance of plants was measured as frequencyof occurrence within sampling quadrats in eachreplicate. A modified quadrat-charting method wasused (Mueller-Dombois & Ellenberg 1974). Thefrequency of herbs in each replicate was determinedwith 15 1 m

�

1 m vegetation quadrats, at regular10 m intervals, with each being subdivided into 1000.01 m

�

0.01 m cells. In each quadrat, the number ofcells occupied by species was used to estimate speciesfrequency per quadrat. Then, the frequency for eachreplicate was estimated by averaging the frequenciesfound in the 15 quadrats. Canopy cover of woodyspecies was estimated within the same 1 m

�

1 mquadrats, and the percentage (0–100%) of quadrats

that were shaded by canopy was used to categorizemicrosites as shaded or exposed. Quadrats were con-sidered to be shaded when the woody species coverwas

�

50%. Species frequencies within each microsite(shaded and exposed) were then calculated.

Soil samples

The seed bank was analysed during late winter 2001(August), late spring 2001 (December) and latesummer 2002 (April), times considered to be criticalperiods (Hoffmann

et al

. 1989). At each samplingtime, 30 soil samples were collected, at 1.5 m intervalsalong randomly placed parallel transects from eachreplicate plot of each successional stage. Fifteensamples were collected underneath the shrub canopyand 15 were taken outside the canopy projection. Thus,540 soil samples were obtained during the study: 30samples

�

2 replicates

�

3 stages

�

3 seasons. Soilsamples were taken with a 5-cm diameter metal borecylinder, dug to a depth of 5 cm. The volume of soil

Table 2.

Herb cover (%) at two microsites in central Chile. Exposed refers to herbs in open microsites, shaded to micrositesunderneath the canopy of shrubs

Species

Winter 2001 Winter 2002

Exposed Shaded Exposed Shaded

Amsinckia calycina

1.3 0.0 8.6 0.0

Anthriscus caucalis

2.5 22.9 7.3 42.2

Bowlesia incana

0.0 0.0 3.0 0.4

Bromus berterianus

46.6 6.1 16.4 0.0

Capsella bursa-pastoris

0.3 0.0 2.6 0.0

Carduus pycnocephalus

< 0.1 0.0 0.0 0.0

Cardamine hirsuta

0.0 0.0 0.7 4.2

Chaetanthera ciliata

0.0 0.0 < 0.1 0.0

Clarkia tenella

0.0 0.0 3.1 0.0

Coniza

sp. 0.0 0.0 1.4 0.0

Cotula australis

0.0 0.0 14.0 0.0

Erodium cicutarium

10.3 0.0 14.5 0.0

Erodium moschatum

0.1 0.0 1.5 0.0

Galium aparine

0.0 0.0 1.0 0.0

Gamochaeta stachydifolia

0.0 0.0 2.0 0.0

Geranium robertianum

0.0 0.0 2.0 0.0

Lactuca serriola

0.0 0.0 0.2 0.0

Leucheria

sp. 1.4 0.0 0.0 0.0

Pectocarya linearis

2.1 0.0 0.0 0.0

Phacelia brachyantha

1.4 0.0 0.0 0.0

Plagiobothrys myosotoides

< 0.1 0.0 < 0.1 0.0

Plantago

sp. < 0.1 0.0 0.0 0.0

Moscharia pinnatifida

2.1 0.0 0.2 0.0

Stellaria abortiva

0.0 0.0 0.0 0.2

Stellaria media

0.0 0.7 0.0 2.2

Trifolium glomeratum

< 0.1 0.0 < 0.1 0.0

Trifolium

sp. 0.0 0.0 0.0 1.0

Vulpia bromoides

4.5 0.0 30.0 1.0Unidentified geophyte 1.3 0.5 3.0 2.0Species total 16.0 4. 21.0 8.


collected was about 200 cm

3

. We focused on the surfacestratum of the seed bank because this horizon generallyholds most of the easily germinating seeds (Buhler1995).

Germination assays

The seed bank was investigated by germinating seedsin all soil samples. Samples were placed over a 2-cmdeep coarse sand layer in about 500 cm

3

plastic trays.These were held in a greenhouse with 12 : 12 photo-period, and with mean temperatures of 25

�

C insummer and 15

�

C during winter. Samples werewatered and checked for emerging seedlings daily,for 60 days. After 60 days there was negligible seedgermination in our soil samples. Thus, the number ofgerminating seeds per species per m

2

of soil wasdetermined. In cases where identification to specieslevel was dubious, seedlings were grown until flower-ing. Nomenclature follows Marticorena and Quezada(1985). The direct germination method provided amore complete list of floristic richness than visualexamination of seeds because it enabled identificationof species with small and light-coloured seeds, whichare difficult to detect in elutriated samples (Gross1990). However, the germination method mayunderestimate the total seed bank (Ter Heerdt

et al.1999), particularly the persistent seed bank and themost common species (Thompson & Grime 1979).Nevertheless, Gross (1990) showed that seeds of themost common species obtained by elutriated samplehad low viability. When this author adjusted the seeddensities in the elutriated sample for the observedmean viability, no statistical difference for seeddensity was found between the two methods. If seedsof some matorral species were dormant, dormancyprobably would have been broken by seasonal thermalvariations, to which all mediterranean environments

are subject (Baskin & Baskin 1989; Ren & Abbot1991; Bell et al. 1993; Skordilis & Thanos 1995;Vázquez-Yanes & Orozco-Segovia 1998). Because soilsamples used for germination tests were collectedduring three consecutive seasons (winter, spring andsummer), it is likely that seeds of any species that hadonly recently been dispersed, or were lying dormant,would have been detected during one of the other twoseasons.

Statistics

For statistical analyses, numbers of seeds from soilsamples obtained from shaded and exposed micrositeswere averaged for comparisons among seasons andamong successional ages after fires. Seed bank densitywas analysed using repeated-measures ANOVA.Microsite (underneath vs outside the canopy) andsuccesional age (young vs intermediate vs maturevegetation) were used as between-subject sources ofvariation, and season (late winter, late spring, latesummer) was used as a within-subjects source ofvariation (Systat 1996). Before conducting statisticalanalyses, seed density data were transformed to ln(x + 1). Repeated-measures ANOVAs were performedon all species, on grasses only, and on all herbs exclu-ding grasses. To determine temporal association (forthe same season) between above-ground vegetationand seed bank, we analysed the relationship betweenthe frequency of established above-ground speciesduring late winter 2001 and their seed density in theseed bank during late winter 2001. To determine intra-annual temporal association (for different seasons)between above-ground vegetation and seed density inthe seed bank, we analysed the relationship between theseed bank during late summer 2002 and frequency ofabove-ground species during the preceding winter.Both were analysed with Spearman’s rank order

Table 3. Repeated-measures ANOVA for the effect of microsite and patch age on total seeds, grasses only and total less grassseeds over time. Seed density comparisons were carried out in ln-transformed data

VariableTotal seed Grass seed Total less grass seed

df F P F P F P

Between-subjects sourceMicrosite (exposed, shaded) 1 9.16 < 0.05 35.96 < 0.01 3.06 NSPatch age 2 2.94 NS 19.97 < 0.01 1.12 NSMicrosite � patch age 2 1.01 NS 15.28 < 0.01 0.60 NSError 6Within-subjects sourceSeason of the year 2 113.17 < 0.001 36.00 < 0.001 92.92 < 0.001Season of the year � Microsite 2 15.73 < 0.01 12.70 < 0.01 3.41 NSSeason of the year � Patch age 4 2.44 NS 2.78 NS 3.95 < 0.05Season of the year � Microsite � Patch age 4 1.82 NS 2.54 NS 1.30 NSError 12

NS, not significant (P > 0.05).

578 J. A. FIGUEROA ET AL.

correlation. For these analyses the species were pooledaccording to microsite (away from vs below thecanopy), because no statistical relationship withsuccessional stage was found.

RESULTS

Frequency and richness of plant species

A total of 17 herb species were recorded during winter2001, 16 of which were found in exposed microsites(Table 2). The annual grass Bromus berterianus wasthe dominant species at exposed microsites, with afrequency of 46.6% during this season (Table 2). Incontrast, at shaded microsites, only four herb speciesoccurred, with a high frequency of Anthriscus caucalis(22.9%).

Twenty-four herbaceous species were recordedduring winter 2002, 21 of which were found atexposed microsites and only eight at shaded microsites(Table 2). The vegetation at exposed microsites wasdominated by four species (B. berterianus, Cotulaaustralis, Erodium cicutarium and V. bromoides), andby only one species (A. caucalis) under the canopy.

Richness of seed bank species

A total of 64 plant species were recorded in the seedbank (for the species list, please Email J. A.Figueroa:[email protected]). Eight of these wereperennial herbs (e.g. Chenopodium ambrosioides,Conyza consanguinea, Gamochaeta stachydifolia,Gnaphalium philippi) and another eight were woodyspecies (e.g. Corynabutilon ceratocarpum, Lithreacaustica, Muehlenbeckia hastulata, Retanilla trinervia).Forty-four species were mainly forb annual/biannualspecies, of which only 16 were native. The remainingfour taxa were identified to genus only.

In young-aged successional stages, 43 plant specieswere recorded in the seed bank throughout the study.Fourteen species were found during late winter, 24during late spring, and 29 during late summer. Thefrequency distribution of species richness in the seedbank for the three seasons did not differ significantlyfrom a uniform frequency distribution (�2 = 3.6;d.f. = 2; P = 0.16). Seeds of only two woody species,Baccharis spp. and Solanum ligustrinum, were collectedin the soil of young-aged patches.

At intermediate-aged successional stages, 47 plantspecies were collected throughout the study. Eightspecies were recorded during late winter, 23 during latespring, and 38 at the end of summer. The frequencydistribution of species richness in the seed bankdiffered significantly from that expected under auniform frequency distribution (�2 = 13.8; d.f. = 2;P < 0.01). Seeds of only three woody species, Lithreacaustica, Podanthus mitiqui and Retanilla trinervia, werefound in this seed bank.

At mature successional stages, 45 plant species werefound in the seed bank. Fifteen species were recorded

Fig. 2. Seed density in the soil for (a) all seeds, (b) grassseeds only, and (c) for all seeds excluding grasses, over time.Bars indicate �1 SE. Dissimilar letters indicate significantdifferences at P < 0.05.


during late winter, 25 during late spring, and 29 duringlate summer. The frequency distribution for the threeseasons did not differ from a uniform frequencydistribution (�2 = 3.2; d.f. = 2; P = 0.21). Seeds ofonly three woody species, Corynabutilon ceratocarpum,Lithrea caustica and Muehlenbeckia hastulata, werecollected in these samples.

Variation and seed bank density

Seed bank density was significantly higher during latespring and summer than during late winter (Table 3).At the end of spring, mean seed density was 20 timeshigher than at the end of winter (Fig. 2a). The grassesBromus berterianus and Vulpia bromoides were the twospecies that contributed most towards the rise in seeddensity. Together, they made up 29% of the totalnumber of seeds in the bank at the end of winterand 84% at the end of spring. The accumulateddensity of these two grasses reached 6000 seeds perm2 during late spring, significantly larger than the369 seeds per m2 reached at the end of winter orthe 1780 seeds per m2 in the late summer (Fig. 2band Table 3). The accumulated density of allremaining species combined, excluding grasses, wassignificantly greater during late summer (Fig. 2c andTable 3).

Total seed density, and grass seeds, within the soilwere significantly greater in exposed than shadedmicrosites (Table 3). In contrast, seed density of allother species combined did not differ significantlybetween the two microsites (Table 3).

Successional age following fires had a significanteffect on seed density, but only with regard to grassseeds. The density of grass seeds in the shaded micro-

sites of mature patches remained low throughoutthe year (< 17 seeds per m2), constituting the onlysignificant interaction between microsite and succes-sional age (Fig. 3, Table 3). Differences in total seeddensity between shaded and exposed microsites variedwith season, as indicated by a significant season–microsite interaction (Table 3). Only in late spring2001 was the total seed density at exposed micrositessignificantly greater than at shaded microsites (Fig. 4).This may be because grass seeds accumulated mainlyduring late spring 2001 and non-grass seeds accumu-lated throughout late summer (see Fig. 2b,c). Specific-ally, the grass seed bank at the end of summer declinedsignificantly in exposed microsites, and accumulatedunder the canopy until late summer (see Fig. 5).

Likewise, successional age showed interaction withseason, only when grasses were excluded from theanalysis of seed bank variation (Table 3). Only duringlate winter, seed bank density (excluding grasses)decreased to a significantly greater extent at inter-mediate- and mature-aged successional stages (Fig. 6).However, during late spring and summer, seed bankdensity did not differ significantly among patches(Fig. 6). Finally, within-subject interactions amongseason, microsite and successional age were notdetected (Table 3).

Above-ground vegetation versus seed bank

The most frequent established woody species wereeither rarely recorded or not recorded at all in the seedbank (e.g. Colliguaja odorifera, Quillaja saponaria,Baccharis spp., Kageneckia oblonga). Nevertheless, allwoody species detected in the seed bank, with theexception of Calceolaria thyrsiflora and Corynabutilonceratocarpum, were observed among the establishedwoody vegetation.

Fig. 3. Mean density of grass seeds in the soil at young,intermediate, and mature successional stage following fires,according to microsites. (�) covered, (�) exposed. Barsindicate �1 SE. Dissimilar letters indicate significantdifferences at P < 0.05.

Fig. 4. Seed density of all seeds in the soil over time andaccording to microsite. (�) exposed, (�) shaded. Bars indi-cate �1 SE. Dissimilar letters indicate significant differencesat P < 0.05.


The seed abundance of species in the seed bank thathad accumulated by late winter 2001 was uncorrelatedwith the frequency of established above-groundspecies in winter 2001, either at exposed or shadedmicrosites (Spearman’s rank order correlation coeffi-cient; r = –0.26; P = 0.22 and r = –0.19; P = 0.44,respectively). Similarly, the seed abundance of speciesin the seed bank by the end of summer 2002 wasuncorrelated with the frequency of established above-ground species in winter 2002, either at exposed orshaded microsites (r = 0.08; P = 0.54 and r = 0.13;P = 0.33, respectively).

DISCUSSION

Richness and function of the seed bank

A wide variety of species (64) were found in the seedbank of the Chilean matorral. However, only five herbspecies dominated the seed bank during most of theyear. Further, the density of the reserve of seeds ofannual grasses, which dominated the herbaceousstratum throughout most of the year, was two ordersof magnitude greater than that of the remainingherbaceous and woody species by the end of spring.Finally, perennials contributed less to seed bankabundance and species richness. These observationsagree with studies in mediterranean (Levassor et al.1990; Jiménez & Armesto 1992; Peco et al. 1998), andsemiarid regions of South America (Bertiller 1998;Gutiérrez et al. 2000; Marone et al. 2000a; Gutiérrez &Meserve 2003), showing that the seed bank is domin-ated by annuals, with short-lived perennial herbs repre-sented in intermediate numbers, and with long-livedwoody species poorly represented. The large seeds of

long-lived species are more likely to suffer predation inthe soil than are small seeds of short-lived plants(Bertiller 1998). Additionally, the lower seed produc-tion, higher seed retention in the canopy, and scarcepresence in the seed rain of long-lived species, may alsocontribute to their infrequent occurrence in the soil(Kemp 1989; Jiménez & Armesto 1992; Bertiller1998).

Among annuals, we found more grass seeds thanforb and leguminous seeds. The same pattern wasfound in California (Major & Pyott 1966). However, inthe seed bank of annual plants in the Mediterraneanbasin (Russi et al. 1992a,b; Peco et al. 1998; Valbuena& Trabaud 2001) and in semiarid South America(Marone et al. 2000a; Gutiérrez et al. 2000), legu-minous and forb seeds, respectively, are the mostfrequent.

The composition, size and dynamics of the seedbank in Mediterranean-type communities are affectedby the persistence of the seeds buried in the soil (Parker& Kelly 1989). In the same way, the seed bank in theChilean matorral is functionally similar to that of soilsundisturbed by fire in the chaparral of California(Parker & Kelly 1989), in Mediterranean basin grass-lands (Russi et al. 1992a; Peco et al. 1998), and incentral Chilean grasslands (Olivares et al. 1994), all ofwhich are dominated by transient seeds. However, thissite differs from the semiarid matorral of north-centralChile and the alpine vegetation in the central ChileanAndes, where a long-lived seed bank prevails (Vidiella& Armesto 1989; Arroyo et al. 1999).

Temporal variation of the seed bank

Herbaceous seeds are a highly dynamic component ofthe seed bank, which in the Chilean matorral reach a

Fig. 5. Seed density of grasses in the soil over time andaccording to microsite. (�) exposed, (�) shaded. Bars indi-cate �1 SE. Dissimilar letters indicate significant differencesat P < 0.05.

Fig. 6. Seed density in the soil (excluding grasses) overtime and according to the successional stages, (�) young,( ) intermediate and (�) mature. Bars indicate �1 SE.Dissimilar letters indicate significant differences at P < 0.05.


minimum density in late winter and a maximum inlate spring. Similar dynamics have been recorded inMediterranean grasslands, which are primarily madeup of therophytes (Levassor et al. 1990; Russi et al.1992a; Olivares et al. 1994). The seed dynamics ofdominant herb species together with variations in theabove-ground layer shows that regeneration of theherbaceous vegetation is driven by the production ofannual seeds, with a short-lived reserve of seeds in thesoil. The grass seed bank during summer accumulatedfrom the seed rain of the preceding spring. The non-grass seed bank was less variable in time, such that agreater number of its seeds accumulated during latesummer. These temporal differences between abun-dance and dynamics of annual grass and non-grassseeds may decrease seedling competition between them(Rice & Dyer 2001). Reduction of annual grass seedsduring summer is probably caused by granivores(Russi et al. 1992b; Marone et al. 2000b). Total seedbank reduction during autumn and winter is attribut-able to germination (Russi et al. 1992a) and, to a lesserextent, to losses before emergence, for instance throughseed decay (Roberts 1986) or consumption by grani-vores (López-Calleja 1995; Marone et al. 2000b).

Spatial variation of the seed bank

The grass-only seed bank was affected by microsite(exposed vs shaded), as has been observed insemiarid (Bertiller 1998), and mediterranean ecosys-tems (Zammit & Zedler 1994). The differences in seedaccumulation between microsites may be due todifferential seed availability, germination, flowering,fruiting, seed predation, or seed viability (Ellner &Shmida 1981; Bustamante & Vásquez 1995; López-Calleja 1995; Hunt 2001; Figueroa et al. 2002). In theChilean matorral, the current vegetation is a lowshrubland, where shrub canopies modify the localmicroenvironment and resource availability in the soil.For example, the soil beneath shrubs accumulatesbiomass, receives lower light intensity, has greaterhumidity, and is subjected to moderate temperatures incomparison to exposed microsites away from thecanopy (Del Pozo et al. 1989; Bertiller 1998). Thus,microsites may affect annual grass establishment, andhence its seed bank, due to relatively short seeddispersal distances (Ellner & Shmida 1981; Bertiller1998).

Effects of successional stage on seed bank

Successional stage had an important effect only on themore dynamic element of the seed bank, annualgrasses. Their abundance was strongly reduced underthe canopy of the mature successional stage, which at

our study site had a cover >70%, a height of 5–15 m,and an age of 30–50 years after fire. The microclimaticconditions underneath the mature stage probably donot favour establishment of annual grasses (Bisigato &Bertiller 1999). Further, dispersal of grass seeds fromexposed toward shaded microsites in the mature stagemay be severely limited, a characteristic shared witharid regions (Ellner & Shmida 1981; Bertiller 1998;Bisigato & Bertiller 1999) and California grasslands(Seabloom et al. 2003). On the other hand, succes-sional stages did not influence species richness in theseed bank. This is in contrast to findings in old fields(Falinska 1999) and in Mediterranean basin grasslands(Levassor et al. 1990), where seed bank species rich-ness decreased during succession, and to finding inMediterranean basin forests (Ne’Eman & Izhaki 1999),where richness increases with succession age.

Generally, persistent seed bank species respond tofire disturbances (Parker & Kelly 1989), with fireintensity, duration, season, and frequency havingdifferent effects on transient seed bank (Parker &Kelly 1989). However, the transient seed bank ofChilean matorral did not respond to the fire regimerepresented by the three successional stages analysed.

Above-ground vegetation versus seed bank

There was little similarity between seed bank andabove-ground vegetation in the Chilean matorral. Thisdiscrepancy may be due to the fate of seeds in the soil,such as seed predation (Marshall & Jain 1970; Cook1980; Baskin & Baskin 1989; Louda 1989; Crowley &Garnett 1999; Marone et al. 2000b), vegetative repro-duction (Baker 1989), or temporal and spatial scaleanalysed (Major & Pyott 1966; Arroyo et al. 1999).Our result agrees with those reported in grasslands(Rice 1989; Funes et al. 2001), Mediterranean basinshrubland (Valbuena & Trabaud 2001) and Californianchaparral (Parker & Kelly 1989), where species withtransient seed bank predominate. It has been reportedthat this dissimilarity may be determined by theperennial/annual species ratio (Peco et al. 1998). Inannual grasslands there are high similarities betweenthe seed bank and vegetation composition (Levassoret al. 1990), while in grasslands dominated by perennialgrasses there are low similarities (Thompson & Grime1979; Bakker et al. 1996). In the Chilean matorral,annual species dominate the herbaceous layer, with fewperennial herbs present, that are only important in theseed bank during late summer. Finally, it should benoted that interannual similarity, between current seedbank and above-ground herb layer in the followingyear, was found in a semiarid region of Chile stronglydominated by ephemeral species (Gutiérrez et al.2000). This type of pattern should be explored in thematorral of central Chile.


ACKNOWLEDGEMENTS

J. A. Figueroa was supported by grants from the A. W.Mellon Foundation and the Center for AdvancedStudies in Ecology & Biodiversity, Pontificia Univer-sidad Católica de Chile. This is a contribution to theresearch program of ONG Entorno. Thanks are due toSergio Castro, Alejandro Muñoz, Chris Lusk, MichaelBull and two anonymous referees for their commentson the manuscript.

REFERENCES

Armesto J. J. & Pickett S. T. A. (1985) A mechanistic approachto the study of succession in the Chilean matorral. Rev. Chil.Hist. Nat. 58, 9–17.

Armesto J. J., Vidiella P. E. & Jiménez H. E. (1994) Evaluatingcauses and mechanisms of succession in the Mediterraneanregions in Chile and California. In: Ecology and Biogeographyof Mediterranean Ecosystems in Chile, California, and Australia(eds M. T. K. Arroyo, P. H. Zedler & M. D. Fox)pp. 418–33. Springer-Verlag, New York.

Aronson J., Del Pozo A., Ovalle C., Avendaño J., Lavin A. &Etienne M. (1998) Land use changes and conflicts in centralChile. In: Landscape Degradation and Biodiversity inMediterranean-Type Ecosystems (eds P. W. Rundel, G.Montenegro & F. M. Jaksic), pp. 155–68. Springer-Verlag,Berlin.

Arroyo M. T. K., Armesto J. J. & Villagrán C. (1981) Plantphenological patterns in the high Andean Cordillera ofcentral Chile. J. Ecol. 69, 205–23.

Arroyo M. T. K., Cavieres L. A., Castor C. & Humaña A. M.(1999) Persistent soil seed bank and standing vegetation at ahigh alpine site in the central Chilean Andes. Oecologia 119,126–32.

Arroyo M. T. K., Cavieres L. A., Marticorena C. & Muñoz-Schick M. (1995) Convergence in the Mediterranean florasin central Chile and California: Insights from comparativebiogeography. In: Ecology and Biogeography of MediterraneanEcosystems in Chile, California, and Australia (eds M. T. K.Arroyo, P. H. Zedler & M. D. Fox) pp. 43–88. Springer-Verlag, New York.

Baker H. G. (1989) Some aspects of the natural history of seedbanks. In: Ecology of Soil Seed Bank (eds M. A. Leck, V. T.Parker, R. L. Simpson) pp. 9–24. Academic Press, SanDiego.

Bakker J. P., Bakker E. S., Rosén E., Verweij G. L. & BekkerR. M. (1996) Soil bank composition along a gradient fromdry alvar grassland to Juniperus shrubland. J. Veg. Sci. 7,165–76.

Baskin J. M. & Baskin C. C. (1989) Physiology of dormancy andgermination in relation to seed bank ecology. In: Ecology ofSoil Seed Bank (eds M. A. Leck, V. T. Parker, R. L.Simpson) pp. 53–65. Academic Press, San Diego.

Bell D. T., Plummer J. A. & Taylor S. K. (1993) Seed germin-ation ecology in southwestern Western Australia. Bot. Rev.59, 24–54.

Bertiller M. B. (1998) Spatial patterns of the germinable soil seedbank in northern Patagonia. Seed Sci. Res. 8, 39–45.

Bisigato A. J. & Bertiller M. B. (1999) Seedling emergence andsurvival in contrasting soil microsites in Patagonian Monteshrubland. J. Veg. Sci. 10, 335–42.

Buhler D. D. (1995) Influence of tillage systems on weedpopulation dynamics and management in corn and soybeanin the central USA. Crop Sci. 35, 1247–58.

Bustamante R. O. & Vásquez R. A. (1995) Granivoría enCryptocarya alba (Mol) Looser (Lauraceae): Los efectos deltipo de hábitat y la densidad de semillas. Rev. Chil. Hist. Nat.68, 117–22.

Cook R. E. (1980) The biology of seeds in the soil. In: Demo-graphy and Evolution in Plant Populations (ed. O. T. Solbrig)pp. 107–29. University of California Press, Berkeley.

Crowley G. & Garnett S. (1999) Seeds of the annual grassesSchizachyrium spp. as a food resource for tropical grani-vorous birds. Austral Ecol. 24, 208–20.

D’Angela E., Facelli J. M. & Jacobo E. (1988) The role of thepermanent soil bank in an early stage of a post-agriculturalsuccession in the Inland Pampa, Argentina. Vegetatio 74,39–45.

Del Pozo A., Fuentes E. R., Hajek E. R. & Molina J. D. (1989)Zonación microclimática por efecto de los manchones dearbustos en el matorral de Chile central. Rev. Chil. Hist. Nat.62, 85–94.

Ellner S. & Shmida A. (1981) Why are adaptations for long-rangeseed dispersal rare in desert plants? Oecologia 51, 133–44.

Falinska K. (1999) Seed bank dynamics in abandoned meadowsduring a 20-year period in the Bialowieza National Park.J. Ecol. 87, 461–75.

Figueroa J. A., Muñoz A. A., Mella J. & Arroyo M. T. K. (2002)Pre and postdispersal seed predation in a Mediterranean-type climate montane sclerophyllous forest in central Chile.Aust. J. Bot. 50, 183–95.

Fuentes E. R. (1990) Landscape change in Mediterranean-typehabitats of Chile: patterns and processes. In: ChangingLandscapes: an Ecological Perspective (eds I. S. Zonneveld &R. T. T. Forman) pp. 165–90. Springer-Verlag, Berlin.

Fuentes E. R., Hoffmann A. J., Poiani A. & Alliende M. C. (1986)Vegetation change in large clearings: patterns in the Chileanmatorral. Oecologia 68, 358–66.

Fuentes E. R., Jaksic F. M. & Simoneti J. A. (1983) Europeanrabbits versus native rodents in central Chile: effects onshrub seedlings. Oecologia 58, 411–4.

Fuentes E. R., Otaíza R. D., Alliende M. C. & Hoffmann A. J.,Poiani A. (1984) Shrubs clumps of the Chilean matorralvegetation: structure and possible maintenance mechanisms.Oecologia 62, 405–11.

Funes G., Basconcelo S., Díaz S. & Cabido M. (2001) Edaphicpatchiness influences grassland regeneration from the soilseed-bank in mountain grassland of central Argentina.Austral Ecol. 26, 205–12.

Gross K. L. (1990) A comparison of methods for estimating seednumbers in the soil. J. Ecol. 78, 1079–93.

Groves R. H. (1986) Invasion of Mediterranean ecosystems byweeds. In: Resilience in Mediterranean-Type Ecosystems (edsB. Dell, A. J. M. Hopkins & B. B. Lamont) pp. 129–45. Dr.W. Junk Publishers, Dordrecht.

Gulmon S. L. (1977) A comparative study of the grasslands ofCalifornia and Chile. Flora 166, 261–78.

Gutiérrez J. R., Arancio G. & Jaksic F. M. (2000) Variation invegetation and seed bank in a Chilean semi-arid communityaffected by ENSO 1997. J. Veg. Sci. 11, 641–8.

Gutiérrez J. R. & Meserve P. L. (2003) El Niño effects on soilseed bank dynamics in north-central Chile. Oecologia 134,511–7.

Hoffmann A. J., Liberona F. & Hoffmann A. E. (1998) Distrib-ution and ecology of geophytes in Chile. Conservationthreats to geophytes in Mediterranean-type regions. In:


Landscape Degradation and Biodiversity in Mediterranean-Type Ecosystems (eds P. W. Rundel, G. Montenegro & F. M.Jaksic) pp. 231–53. Springer-Verlag, Berlin.

Hoffmann A. J., Teillier S. & Fuentes E. R. (1989) Fruit and seedcharacteristics of woody species in Mediterranean-typeregions of Chile and California. Rev. Chil. Hist. Nat. 62,43–60.

Holmes P. (2002) Depth distribution and composition of seed-banks in alien-invaded and uninvaded fynbos vegetation.Austral Ecol. 27, 110–20.

Holmgren M., Avilés R., Sierralta L., Segura A. M. & FuentesE. R. (2000) Why have European herbs so successfullyinvaded the Chilean matorral? Effects of herbivory, soilnutrients, and fire. J. Arid Environ. 44, 197–211.

Hunt L. P. (2001) Low seed availability may limit recruitment ingrazed Atriplex vesicaria and contribute to local extinction.Plant Ecol. 157, 53–67.

Jaksic F. M. (2001a) Spatiotemporal variation patterns of plantsand animals in San Carlos de Apoquindo, central Chile. Rev.Chil. Hist. Nat. 74, 477–502.

Jaksic F. M. (2001b) Ecological effects of El Niño in terrestrialecosystems of western South America. Ecography 24,241–50.

Jiménez H. E. & Armesto J. J. (1992) Importance of the soil seedbank of disturbed sites in Chilean matorral in earlysecondary succession. J. Veg. Sci. 3, 579–86.

Keeley S. C. & Johnson A. W. (1977) A comparison of thepattern of herb and shrub growth in comparable sites inChile and California. Am. Midl. Nat. 97, 20–32.

Keeley J. E. & Nitzberg M. E. (1984) Role of charred wood inthe germination of the chaparral herbs Emmenanthe penduli-flora (Hydrophyllaceae) and Eriophyllum confertiflorum(Asteraceae). Madroño 31, 208–18.

Kemp P. R. (1989) Seed bank and vegetation processes ondeserts. In: Ecology of Soil Seed Bank (eds M. A. Leck, V. T.Parker & R. L. Simpson) pp. 257–81. Academic Press, SanDiego.

Leck M. A. (1989) Wetland seed bank. In: Ecology of Soil SeedBank (eds M. A. Leck, V. T. Parker, R. L. Simpson)pp. 283–308. Academic Press, San Diego.

Levassor C., Ortega M. & Peco B. (1990) Seed bank dynamicsof Mediterranean pastures subjected to mechanical distur-bance. J. Veg. Sci. 1, 339–44.

López-Calleja M. V. (1995) Dieta de Zonotrichia capensis y Diucadiuca: Efecto de la variación estacional y la riqueza de avesgranívoras en Chile central. Rev. Chil. Hist. Nat. 68, 321–31.

Louda S. A. (1989) Predation in the dynamics of seed regener-ation. In: Ecology of Soil Seed Bank (eds M. A. Leck, V. T.Parker, R. L. Simpson) pp. 25–51. Academic Press, SanDiego.

Major J. & Pyott W. T. (1966) Buried, viable seeds in twoCalifornia bunchgrass sites and their bearing on thedefinition of a flora. Vegetatio 13, 253–82.

Marone L., Horno M. E. & González del Solar R. (2000a) Post-dispersal fate of seeds in the Monte desert of Argentina:patterns of germination in successive wet and dry years.J. Ecol. 88, 940–9.

Marone L., López de Casenave J. & Cueto V. R. (2000b)Granivory in southern South American deserts: conceptualissues and current evidence. Biosci. 50, 123–32.

Marshall D. R. & Jain S. K. (1970) Seed predation and dormancyin the population dynamics of Avena fatua and A. barbata.Ecology 51, 886–91.

Marticorena C. & Quezada M. (1985) Catálogo de la floravascular de Chile. Gayana Bot. 42, 1–157.

Montenegro G., Teillier S., Arce P. & Poblete V. (1991) Intro-duction of plants into the Mediterranean-type climate areaof Chile. In: Biogeography of Mediterranean Invasions (edsH. Groves & F. di Castri) pp. 103–14. Cambridge UniversityPress, Cambridge.

Mueller-Dombois D. & Ellenberg H. (1974) Aims and Methods ofVegetation Ecology. Wiley & Sons, New York.

Muñoz M. R. & Fuentes E. R. (1989) Does fire induce shrubgermination in the Chilean matorral? Oikos 56, 177–81.

Ne’Eman G. & Izhaki I. (1999) The effect of stand age andmicrohabitat on soil seed banks in Mediterranean Aleppopine forests after fire. Plant Ecol. 144, 115–25.

Olivares A., Johnston M. & Contreras X. (1994) Influencia delestrato arbóreo en la reserva de semillas del suelo. Simiente(Chile) 64, 248–53.

Ortega M., Levassor C. & Peco B. (1997) Seasonal dynamics ofMediterranean pasture seed banks along environmentalgradients. J. Biogeogr. 24, 177–95.

Parker V. T. & Kelly V. R. (1989) Seed bank in Californiachaparral and other Mediterranean climate shrublands.In: Ecology of Soil Seed Bank (eds M. A. Leck, V. T.Parker & R. L. Simpson) pp. 231–56. Academic Press,San Diego.

Parker V. T., Simpson R. L. & Leck M. A. (1989) Pattern andprocess in the dynamics of seed banks. In: Ecology of Soil SeedBank (eds M. A. Leck, V. T. Parker & R. L. Simpson)pp. 367–84. Academic Press, San Diego.

Peco B., Ortega M. & Levassor C. (1998) Similarity betweenseed bank and vegetation in Mediterranean grassland: apredictive model. J. Veg. Sci. 9, 815–28.

Pugnaire F. & Lázaro R. (2000) Seed bank and understoreyspecies composition in a semi-arid environment: the shrubage and rainfall. Ann. Bot. 86, 807–13.

Ren Z. & Abbot J. R. (1991) Seed dormancy in MediterraneanSenecio vulgaris L. New Phytol. 117, 673–8.

Rice K. J. (1989) Impacts of seed banks on grassland communitystructure and population dynamics. In: Ecology of Soil SeedBank (eds M. A. Leck, V. T. Parker & R. L. Simpson)pp. 211–30. Academic Press, San Diego.

Rice K. J. & Dyer A. R. (2001) Seed aging, delayed germinationand reduced competitive ability in Bromus tectorum. PlantEcol. 155, 237–43.

Roberts H. A. (1986) Quantifying seed deterioration. In:Physiology of Seed Deterioration (eds M. W. McDonald &C. J. Nelson) pp. 101–23. Crop Science Society of America,Madison.

Russi L., Cocks P. S. & Roberts E. H. (1992a) Seed bankdynamics in a Mediterranean grassland. J. Appl. Ecol.29, 763–71.

Russi L., Cocks P. S. & Roberts E. H. (1992b) The fate oflegume seeds eaten by sheep from a Mediterranean grass-land. J. Appl. Ecol. 29, 772–8.

Seabloom E. W., Border E. T., Boucher V. L. et al. (2003)Composition, seed limitation, disturbance, and reestablish-ment of California native annual forbs. Ecol. Appl. 13,575–92.

Skordilis A. & Thanos C. A. (1995) Seed stratification andgermination strategy in the Mediterranean pines Pinus brutiaand P. halepensis. Seed Sci. Res. 5, 151–60.

Systat (1996) Statistics version 6.0. Systat Inc, Evanston.Ter Heerdt G. N. J., Schutter A. & Bakker J. P. (1999) The effect

of water supply on seed-bank analysis using the seedling-emergence method. Funct. Ecol. 13, 428–30.

Thompson K. (1986) Small-scale heterogeneity in the seed bankof an acidic grassland. J. Ecol. 74, 733–8.


Thompson K. & Grime J. P. (1979) Seasonal variation in the seedbank of herbaceous species in ten contrasting habitats.J. Ecol. 67, 893–921.

Valbuena L. & Trabaud L. (2001) Contribution of the soil seedbank to post-fire recovery of a heathland. Plant Ecol. 152,175–83.

Vázquez-Yanes C. & Orozco-Segovia A. (1998) Physiologicalecology of Mediterranean seeds: links with ex situ conserv-ation of plants. In: Landscape Degradation and Biodiversity in

Mediterranean-Type Ecosystems (eds P. W. Rundel, G.Montenegro & F. M. Jaksic) pp. 265–72. Springer-Verlag,Berlin.

Vidiella P. E. & Armesto J. J. (1989) Emergence of ephemeralplant species from soil samples in the Chilean coastal desertin responses to experimental irrigation. Rev. Chil. Hist. Nat.62, 99–107.

Zammit C. & Zedler P. H. (1994) Organization of the soil seedbank in the mixed chaparral. Vegetatio 111, 1–16.

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Composition, size and dynamics of the seed bank in a mediterranean shrubland of Chile