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Acta Oecologica 49 (2013) 116e124

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Acta Oecologica

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Original article

Fire occurrence and tussock size modulate facilitation byAmpelodesmos mauritanicus

Guido Incerti, Daniele Giordano, Adriano Stinca, Mauro Senatore, Pasquale Termolino,Stefano Mazzoleni, Giuliano Bonanomi*

Dipartimento di Agraria, University of Naples Federico II, via Università 100, Portici 80055, NA, Italy

a r t i c l e i n f o

Article history:Received 12 June 2012Accepted 24 March 2013Available online

Keywords:Central die-backCompetitionPlant-soil feedbackRing-forming perennial grass

* Corresponding author. Tel.: þ39 081 2539015.E-mail address: giuliano.bonanomi@unina.it (G. B

1146-609X/$ e see front matter � 2013 Elsevier Mashttp://dx.doi.org/10.1016/j.actao.2013.03.012

a b s t r a c t

Facilitation has been reported for a wide range of plant communities, with evidence of interactionsbetween protégé and nurse plants shifting during their ontogenetic cycles. This study showed that largeAmpelodesmos mauritanicus tussocks can act as nurse for different species, but only after fire occurrence.Large tussocks are typically composed by an external belt of living tillers surrounding dead standingtillers in the inner area, thus being arranged as a “ring” shape. A low plant diversity in unburned sites,dominated by intact Ampelodesmos tussocks, was related to the intense aboveground competition due tospace physical limitation by standing tillers, as well as to the reduction of light availability at groundlevel. In contrast, after burning, tussocks resprouted only in their external belts, leaving empty innerareas. During post-fire recovery, several species (e.g. Plantago spp., Trifolium spp., Carlina spp.) recolonizethe bare soil among different tussocks. On the other hand, a moss (Funaria hygrometrica) and severalherbaceous and woody plants (e.g. Spartium junceum, Calicotome villosa, Quercus pubescens subsp.pubescens) were selectively distributed within the ash-full central areas of burned Ampelodesmos tus-socks. In summary, the study reported evidence of changing prevalence in the interplay of competitionand facilitation effects between small and large Ampelodesmos tussocks, respectively. These resultssuggest a broad significance of the interactions between fire occurrence and ontogenetic phases of thedominant species in affecting the restoration dynamics of natural plant communities.

� 2013 Elsevier Masson SAS. All rights reserved.

1. Introduction

Facilitative interactions mediated by environmental changeshave been recognized as a main driver in shaping natural plantcommunities (Callaway, 2007). Planteplant facilitation has beenreported worldwide in a variety of ecosystems, including deserts(Yeaton, 1978), Mediterranean maquis (Gómez-Aparicio et al.,2004), grazed grasslands (Bonanomi et al., 2005), freshwater andsaline wetlands (Adema and Grootjans, 2003; Bertness and Hacker,1994), as well as alpine ecosystems (Callaway et al., 2002).

The mechanisms underlying facilitative interactions depend onthe specific nurseeprotégé combination and by environmentalconditions (Bonanomi et al., 2011). Callaway (2007) classifiedfacilitation mechanisms as either direct, when a beneficiary isfacilitated through themodification of environmental conditions ornutrient enrichment due to the nurse, or indirect, when the processrequires an intermediating species. In semiarid environments,

onanomi).

son SAS. All rights reserved.

mechanisms of facilitative interactions include the reduction ofexcessive direct solar radiation by shading (Lenz and Facelli, 2003),the buffering of high temperatures (Steenbergh and Lowe, 1969),the local increase of soil resources such as nitrogen and water(Pugnaire et al., 1996; Bonanomi et al., 2008), the protection byunpalatable plants from grazing (Baraza et al., 2006), salinityreduction (Bertness and Shumway, 1993), and substrate stabiliza-tion (Crain and Bertness, 2005). Accumulating evidence indicatesthat facilitation and competition operate simultaneously, thusaffecting the final outcome of planteplant interactions in semi-aridenvironments (Holmgren et al., 1997; Holzapfel and Mahall, 1999).However, the interplay between facilitation and competition canshift during the ontogenetic life cycle of both nurse and protégéplants (Miriti, 2006; Soliveres et al., 2010). In this context, themajority of available studies focused on the variable effects ofprotégé on nurse plants (for a review see Bonanomi et al., 2010).Such studies often reported that once the protégé plant is mature,the interaction with the nurse can shift from commensalic tocompetitive (McAuliffe, 1988; Valiente-Banuet and Ezcurra, 1991;Flores-Martinez et al., 1994). In contrast, only few studies addressedthe changes of beneficial effects related to the canopy of nurse plant

G. Incerti et al. / Acta Oecologica 49 (2013) 116e124 117

during its ontogenetic cycle. A notable exception is the study byFacelli and Brock (2000), reporting that the nurse capability ofAcacia papyrocarpa is related to below-canopy concentration oforganic matter, N, P, and S, progressively increasing with tree ageand slowly declining after its death, over a time span of centuries.More recently, Reisman-Berman (2007) reported that the facilita-tive effect of the spiny shrub Sarcopoterium spinosum on conspecificrecruitment showed an unimodal pattern in relation to canopydensity and shrub age. Potential nurse plants to effectively facilitateother plant require specific morphological traits and an adequatesize to provide shade and/or protect from wind and/or grazing. Inthe case of soil fertility islands under nurse canopies, a time periodsufficiently long for their build-up implies decades or even cen-turies of nurse plants life span.

The final outcome of planteplant interactions can be modulatedby the interplay between abiotic factors during the different phasesof the nurse ontogenetic cycle. For instance, Soliveres et al. (2010)reported that the nursing effect of the perennial grass Stipa tena-cissima on the shrub Lepidium subulatum was modulated by theshrub age and the intensity of abiotic stress. In this context, facili-tation in fire-prone ecosystems has been previously reported withseveral cases of inter- and intra-specific positive interactions due tothe so-called “fireegrass cycle” where the large accumulation ofeasily burnable above-ground litter enhances the system flamma-bility (D’Antonio and Vitousek, 1992). As a consequence of theincreased fire frequency, potential competitors (mainly shrubs andtrees) are out competed due to the higher post-disturbance re-covery ability of the grasses. However, there is no evidence that fireoccurrence may modify the capability of plants to act as nursesduring the different phases of their ontogenetic cycle. Ampelo-desmos mauritanicus (Poir.) T. Durand et Schinz (after here Ampe-lodesmos) is a perennial tussock grass of semi-arid environments,forming fire-prone steppes with very short fire-return intervals(Grigulis et al., 2005). In this study, we explore the relationshipbetween Ampelodesmos and co-occurring plant species taking intoaccount different fire regimes and tussock sizes. This approachprovided the possibility of testing the occurrence of competitiveand facilitative interactions involving Ampelodesmos tussocks atdifferent ontogenetic phases and under different fire conditions.Specifically, we assess that Ampelodesmos tussock may act as anurse, for a range of different species, only if large tussocks aresubject to fire. Specific hypotheses tested were:

(1) Ampelodesmos tussocks largely exclude other species inabsence of fire;

(2) fire occurrence, by determining a competitive release, allowsfacilitative interactions within burned Ampelodesmos tussocks;

(3) Ampelodesmos facilitative effects increase with tussock size;(4) Ampelodesmos seedlings do not establish in the inner area of

burned rings showing a plant-soil negative feedback.

2. Methods

2.1. Plant species and description of study sites

Ampelodesmos is a large tussock grass widespread in the Medi-terranean Basin (Vilà and Lloret, 2000a), currently expanding inareas with high fire frequency because of its rapid and effectivevegetative reproduction after burning, which produces nearlymonospecific stands in sites previously occupied by differentscrubs (Grigulis et al., 2005). At individual level, this grass shows adistinctive centrifugal growth of tillers, rhizomes and roots that intime generates tussocks with a regular “ring” shape (Fig. 1). At thestudy sites, tussocks can attain diameter higher than 1 m, with

flowering and non-flowering stems reaching height of 120 cm andover 250 cm, respectively.

The study was carried out in two sites located in the NationalPark of Cilento e Vallo di Diano, Southern Italy: Punta Tresino,hereafter indicated as the first study site (40�1803900 N e 14�5703800

E; 88 m a.s.l.) and Costa Infreschi, the second study site (40�0004700

N e 15�2501800 E; 285 m a.s.l.). Vegetation in both sites was opengrasslands dominated by Ampelodesmos tussocks (average heightwas 150e200 and 120e150 cm at first and second study sites,respectively), intermingled with herbaceous vegetation and scat-tered shrubs and trees (mainly Calicotome villosa, Myrtus communissubsp. communis, Pistacia lentiscus, Spartium junceum and Quercuspubescens subsp. pubescens). The two sites share a similar Medi-terranean climate with cool, wet winter and warm and dry summerseason. Climatic time series recorded at the closest meteorologicalstation from the two sites, located at Capaccio (14 km NE from thefirst site) and Capo Palinuro (16 km W from the second site),respectively, showed mean annual precipitations of 988 mm and697 mm, monthly temperatures ranging between maxima of24.4 �C and 24.5 �C (August) and 6.8 �C and 10.2 �C (January). Sitesdiffered in geomorphology with sedimentary (flysch) and lime-stone rocks overlying clay soils with abundant rock outcrops at firstand second site, respectively.

2.2. Vegetation survey

Vegetation surveys were carried out to assess the association ofAmpelodesmos with coexisting herbaceous and woody species. Thesampling strategy for vegetation surveys was planned at both studysites considering two main predictive factors for facilitative in-teractions: i. Ampelodesmos tussocks size; ii. time elapsed since thelast wild fire occurrence. Concerning plant size, tussocks wereclassified either as small or large if their external diameter waseither lower or higher than 30 cm (Fig. 1), thus subdividing thereference Ampelodesmos population into two main strata. Weselected 30 cm as a threshold value because it corresponds to anontogenetic shift in tussock structure, which over such limitgenerally begins to show a typical ring shape. Stratificationwas alsoapplied with reference to time elapsed since fire, by separatelyconsidering unburned (at least 10 years since the last fire occur-rence) and burned areas (1.5 years since the last fire occurrence,hereafter indicated as post-fire areas). Three burned and threeunburned sampling areas were randomly selected at each studysite. Overall, 12 sampling areas were selected for vegetation surveys(six for each study site).

In each sampling area 40 Ampelodesmos tussocks (20 small and20 large) were randomly selected, and, for each tussock, twodifferent zones of potential canopy influence were identified atground: the canopy crown area (IN - influenced by living and deadtillers) and the area outside the canopy at a distance of at least50 cm from the nearest tussock (OUT). For each tussock, Ampelo-desmos living biomass (g) and litter mass (g), as well as totalvegetation cover (% of sampled area), biomass (g) and speciesrichness of plant community were assessed during the growingseason in AprileJune of 2007, after randomly placing squaredsampling frames (20� 20 cm) inside (IN; n¼ 20) and outside (OUT;n ¼ 20) small (n ¼ 20) and large (n ¼ 20) tussocks. Overall, 480Ampelodesmos tussocks were analyzed (40 tussocks � 6 studyareas � 2 study sites).

The above-ground living plant biomass within the samplingframes was cut with scissors and harvested. The collected above-ground biomass was sorted into dead litter and living material ofmosses and vascular plants, and separated for each species. Theplants were identified according to Pignatti (1982). Living biomassand litter mass for each species was expressed as dry weight after

Fig. 1. Example of Ampelodesmos tussocks considered in the vegetation surveys of unburned and burned areas. Sampling plots were located inside (IN) and outside (OUT) theindividual tussocks. Post-fire resproutings of large tussocks are typically “ring” shaped with inner ash accumulation.

G. Incerti et al. / Acta Oecologica 49 (2013) 116e124118

oven drying at 60 �C for 8 days. Total vegetation cover within eachsampling frame was visually estimated, as well as the occurrencesof all shrub and tree seedlings.

Significant differences of plant cover, species richness, and plantbiomass between inside and outside Ampelodesmos tussocks, aswell as between small and large tussocks, either in unburned areasor in post-fire conditions were tested with ANOVA statistics usingthe software package STATISTICA 7 (Stat-Soft Inc., US).

2.3. Environmental parameters

The following abiotic parameters were measured to support acorrelative approach to vegetation survey data. Photosyntheticactive radiation (PAR, wavelength between 400 and 700 nm) wasmeasured (instrument ADC-L2A light sensor) at a height of 0, 20,40, 60, 80 and 100 cm above the ground, under the canopy of 20randomly selected Ampelodesmos tussocks at each study site.Measurements were done inside small (IN small) and large (INlarge) Ampelodesmos tussocks, as well as outside the canopy(OUT) under bright, sunny conditions around mid-day in June2011.

The soil was sampled during the growing season (May 2007)considering a single layer corresponding to Ampelodesmos rootdepth (0e20 cm) under the selected tussocks. Soil samples weresieved (mesh size 2 mm) and analyzed for pH, salinity (EC), organicmatter content, total N, exchangeable Caþþ, and bulk density. For allchemical analyses the official methods of the Italian National So-ciety of Soil Science were used (Violante, 2000).

Significant differences of environmental conditions related totussock size, zone, and fire regime were tested with ANOVA sta-tistics using the software package STATISTICA 7 (Stat-Soft Inc., US).

3. Results

3.1. Tussock structure, plant cover and species diversity

Ampelodesmos tussocks showed a consistent spatial pattern ofliving and dead tillers in relation to plant size and fire occurrence.Small tussocks were almost exclusively composed of living tillersindependent of fire occurrence (Figs. 1 and 2). In contrast, tillerswere absent from the inner zone of large tussocks in burned areas,whereas dead, standing tillers were abundant within large tussocksin unburned areas (Figs. 1 and 2). This distribution pattern reflectsthe centrifugal growth of individual rhizomes generating thetypical “ring” shape of the tussocks: a central area without tillerssurrounded by a ring with high tiller density (Fig. 1). Ampelodesmosliving biomass was higher in large unburned tussocks and lower insmall burned plants (Fig. 2). Such differencewas farmore evident inthe case of standing litter, with litter accumulation in large un-burned tussocks being one order of magnitude higher than in theother tested conditions (Fig. 2).

Light attenuation through the canopy of Ampelodesmos tussockswas consistent along the vertical profile of measurements, but withremarkable differences among the tested conditions (Fig. 2). Thelowest PAR values were found inside large unburned tussocks,while a significant, but less consistent pattern occurred inside smalltussocks and large burned ones (Fig. 2; one-way ANOVA, P < 0.05;PAR values at ground level were OUTUNBURNED ¼ 564 � 123a;OUTBURNED ¼ 690 � 110a; INLARGE UNBURNED ¼ 16 � 20c; INLARGE

BURNED ¼ 541 � 156 ab; INSMALL UNBURNED ¼ 72 � 44c; INSMALL

BURNED ¼ 462 � 98b; mmol photon m�2 s�1).Vegetation cover and species diversity were similarly affected by

fire occurrence at both study sites, both considering data recorded

Fig. 2. Living biomass and standing litter of Ampelodesmos individuals at two study sites according to tussock size and fire occurrence (top), and corresponding PAR attenuationalong the vertical profiles inside and outside the tussocks canopy (bottom).

G. Incerti et al. / Acta Oecologica 49 (2013) 116e124 119

inside and outside Ampelodesmos tussocks (Fig. 3). In absence offire, the cover of all plant species, excluding Ampelodesmos, wasquite low, with minimal values in the inner tussock areas, andmaximal outside the tussocks (Fig. 3). Noticeably, in unburnedareas of both study sites, no heterospecific plants were found insidelarge Ampelodesmos tussocks, with consequent null plant diversityand cover (Fig. 3). However, in post-fire conditions, a significantvegetation recovery was observed in both study sites (Fig. 3). Totalplant cover was highest outside tussocks, whereas lower values

Fig. 3. Vegetation cover and species richness outside (OUT) and inside (IN) differently sized Ato means þ1SE. Different letters indicate statistically significant between-group differences

were observed inside large and small Ampelodesmos tussocks, thelatter showing the lowest percent cover (Fig. 3).

Species richness inside and outside Ampelodesmos tussocksfollowed a pattern similar to that of plant cover. In detail, unburnedareas showed generally low values, relative maxima outside thetussocks, intermediate values inside small tussocks and nulls insidelarge tussocks (Fig. 3). In contrast, diversity was much higher inpost-fire conditions (Fig. 3). In general, differences between studysites were minimal. At the first study site species richness was

mpelodesmos tussocks in either unburned or burned areas at two study sites. Data referwithin each fire regime (ANOVA Duncan test; P < 0.05).

G. Incerti et al. / Acta Oecologica 49 (2013) 116e124120

higher outside and lower inside tussocks, with large and smalltussocks showing higher and lower values, respectively (Fig. 3).Differently, at the second study site, similar values of species rich-ness were found outside and inside large tussocks, being signifi-cantly higher than inside small tussocks (Fig. 3).

3.2. Species association with Ampelodesmos tussocks

Overall, 40 and 30 species were recorded at the first and secondstudy sites, respectively (Tables 1 and 2). Most of the species areeither annual or perennial grasses, but seedlings of shrubs and treeswere also found, with 7 and 5 woody species recorded at the firstand second sites, respectively. Two moss species were also recor-ded (Tables 1 and 2).

Most of the plant and moss species were not uniformly distrib-uted around Ampelodesmos tussocks, with selective spreadingdepending on fire conditions and tussock size. At both sites, in

Table 1Plant species distribution outside (OUT) and inside either small (IN small, diameter< 30 cfirst study site (Punta Tresino). Data refer to mean biomass (g per plot of 400 cm2) for all hplants. Small letters indicate statistically significant between-group differences within eaitalic and bold type (ANOVA Duncan test; P < 0.05). Zero values and corresponding lette

Species Unburned areas

OUT IN small

MossesFunaria hygrometrica e e

Unidentified moss_1 e e

Herbaceous annualAira elegantissima e e

Blackstonia perfoliata 0.6 b e

Centaurium erythraea e e

Crepis vesicaria subsp. Vesicaria e e

Cynosurus echinatus e e

Galactites elegans e e

Gastridium ventricosum e e

Medicago minima e e

Melilotus indicus 5.3 b e

Scorpiurus muricatus e e

Trifolium angustifoliumsubsp. angustifolium

e e

Trifolium arvense subsp. arvense e e

Trifolium campestre 0.9 b e

Vicia spp. e 2.3 bUnidentified Asteracea_1 e e

Unidentified Asteracea_2 e e

Unidentified grass_1 e e

Unidentified grass_2 2.3 b e

Herbaceous perennialAmpelodesmos mauritanicusa e e

Briza media e e

Carex sp. 10.2 b e

Carlina sp. 17.5 b e

Dactylis glomerata subsp. glomerata 0.2 a 14.3 bDaucus carota e e

Eryngium amethystinum 2.1 b e

Euphorbia sp. e e

Hypochaeris radicata e e

Mentha sp. e e

Plantago lanceolata 0.3 b e

Plantago serraria 4.3 b e

Pulicaria odora 15.0 b e

Shrub & treeAsparagus acutifolius e e

Calicotome villosa e e

Helichrysum italicum subsp. italicum e e

Myrtus communis subsp. communis e e

Pistacia lentiscus e e

Quercus pubescens subsp. pubescens e e

Spartium junceum e 0.9 b

a For Ampelodesmos mauritanicus data refer to biomass of seedling recruitment.

absence of fire no species were exclusively associated to large tus-socks, and only few species (e.g. Dactylis glomerata subsp. glomerata,Latyrus sp., Vicia sp.) were significantly more abundant in smalltussocks (Tables 1 and 2). An opposite patternwas found in post-fireconditions, with 21 and 12 species exclusively or preferentiallyassociated with large Ampelodesmos tussocks at the first and secondstudy sites, respectively (Tables 1 and 2). In detail, at the first site themoss Funaria igrometricawas exclusively found inside large tussocks(Table 1) where also some herbaceous species were significantlymost abundant (e.g. Aira elegantissima, Stellaria media subsp.media).Many other herbaceous species preferentially occurred outsideAmpelodesmos tussocks, at both study sites (Tables 1 and 2),including Plantago species (Plantago lanceolata and Plantago serra-ria). Interestingly, few Ampelodesmos seedling recruitments wererecorded, none of which inside established tussocks of conspecifics(Tables 1 and 2). Several other species were preferentially distrib-uted outside Ampelodesmos tussocks, including Pulicaria odora and

m) or large (IN large,> 30 cm) Ampelodesmos tussocks in relation to fire regime at theerbaceous species and seedling abundance (number of individuals per m2) for woodych fire regime. Significant differences between fire regimes within each group are inrs (a) are omitted to improve readability.

Burned areas

IN large OUT IN small IN large

e e e 31.4 be 1.2 b e e

e 0.1 b e 1.3ce 0.2 a e 2.9 be 1.4 b e 0.1 ae 1.5 b e e

e 0.5 b 0.1 a 7.1 ce 12.4 c e 5.7 be 2.4 b e 16.5 ce e e 0.6 ae 1.0 b e e

e 3.1 c e 0.3 be 2.2 b e 6.8 c

e 0.6 a 0.3 a 14.6 be 10.4 c e 5.8 be 0.9 b 2.0 a 5.9 ce 0.1 a e 26.1 be 0.4 b e e

e 0.1 b e 3.7 ce 35.1 c e 11.2 b

e 2.3 b e e

e 0.2 b e 4.2 ce 16.5 c 1.3 a 10.5 be 22.3 b e 19.4 b0.4 a e 29.6 b 3.6 ae 0.9 a 0.3 a 13.9 be 19.3 b 0.4 a 1.1 ae 0.3 b e e

e 0.9 a 0.6 a 5.8 be e 0.9 b e

e 26.3 b e e

e 98.6 b e e

e 13.0 b e e

0.2 a e e 1.2 be 0.4 a e 3.4 be e e 0.3 ae e e 0.5 be e e 0.9 be e 0.4 a 4.2 be 0.2 a 1.7 a 6.5 b

Table 2Plant species distribution outside (OUT) and inside either small (IN small, diameter<30 cm) or large (IN large,>30 cm) Ampelodesmos tussocks in relation to fire regimeat the second study site (Costa Infreschi). Legends as inTable 1 caption.

Species Unburnt areas Burned areas

OUT INsmall

INlarge

OUT INsmall

INlarge

MossesUnidentified moss_1 e e e e 0.3 a 4.7 b

Herbaceous annualAira elegantissima e e e 0.3 a e 5.3 bAnagallis sp. 0.9 b 1.1 b e 0.2 a 3.4 b 0.1 aAnthyllis sp. e e e 5.0 c 1.4 b 0.2 aAsterolinon linum-stellatum 6.1 b e e 2.7 c 1.1 b e

Blackstonia perfoliata e e e e e 2.3 bBromus hordeaceussubsp. hordeaceus

e e e e e 1.4 b

Catapodium rigidumsubsp. rigidum

1.1 b e e 0.9 b e e

Lathyrus sp. e 5.6 b e e 2.4 b e

Lotus sp. e e e e 3.1 a 2.3 aMedicago minima e e e 0.3 a e e

Melilous indicus e e e 2.2 b e e

Scorpiurus muricatus 0.3 b e e 12.3 b 0.4 b e

Stellaria media subsp. media e e e e 1.3 b 5.7 cTrifolium angustifoliumsubsp. angustifolium

e e e 0.3 a 0.1 a 0.6 a

Trifolium campestre e e e 4.5 b e e

Vicia sp. e 3.2 b e 1.1 b 4.5 c e

Unidentified Asteracea_1 e e e e e 12.1 b

Herbaceous perennialAmpelodesmos mauritanicusa e e e 0.3 b e e

Carex sp. e e e 1.1 b 3.4 c 0.6 aDactylis glomeratasubsp. glomerata

e e e 0.3 a e 0.2 a

Galium sp. e e e 1.1 b e 2.4 cHypericum perforatum 0.8 b e e 0.8 b e e

Plantago lanceolata e e e 1.4 b e e

Plantago serraria 7.1 b e e 25.1 b e e

Shrub & treeAsparagus acutifolius e e e e 0.3 b 0.9 bCalicotome villosa e e e 0.1 a 1.1 b 9.3 cCistus monspeliensis e e e 14.2 b 0.5 a 0.2 aDittrichia viscosa subsp. viscosa e e e e e 0.4 bSpartium junceum e e e e 0.9 b 2.3 c

a For Ampelodesmos mauritanicus data refer to biomass of seedling recruitment.

G. Incerti et al. / Acta Oecologica 49 (2013) 116e124 121

the nitrogen fixing Scorpiurus muricatus, Trifolium campestre andTrifolium capraceus at the first study site, and Melilotus indica, S.muricatus and T. campestre at the second site (Tables 1 and 2).Differently, at the first site A. elegantissima, Blackstonia perfoliata,Gastridium ventricusum, Hypochaeris radicata, Trifolium arvensesubsp. arvense and Trifolium angustifolium subsp. angustifolium andan unidentified asteracea were significantly associated to largetussocks (Table 1), as well as A. elegantissima, B. perfoliata, Galium sp.and an unidentified asteracea at the second site.

Table 3Soil parameters sampled in the top 15 cm of unburned and burned areas under either smaall parameters. Different letters indicate statistically significant between-group differencebold type (ANOVA Duncan test; P < 0.05).

Unburnt areas

OUT IN small

Soil parameter

PH 7.9 � 0.3 a 7.5 � 0.5 aSalinity (mS cm�1) 149 � 44 a 219 � 46 bOrganic carbon (g kg�1) 23.3 � 6 a 17.3 � 5 aTotal N (g kg�1) 2.58 � 0.4 a 2.13 � 0.6 aExchangeable Caþþ (meq 100 g�1) 24.1 � 7.5 a 20.3 � 5.9 aBulk density (g cm�3) 1.15 � 0.1 a 1.14 � 0.2 a

Vine, shrub and tree specieswere all significantly associatedwithlarge burned Ampelodesmos tussocks (Tables 1 and 2), with theexception of Cistus monspeliensis that was more abundant outsidetussocks,. This pattern was especially evident for nitrogen fixingshrubs (Spartium junceum and Calicotome villosa) and the seedlingrecruitments of Q. pubescens subsp. pubescens, which were almostexclusively recorded inside large tussocks (Tables 1 and 2). On thecontrary, unburned tussocks, independent of their size, did notharbour recruitments of vine, shrub and tree species (Tables 1 and2).

3.3. Environmental parameters

Irrespective of fire occurrences, the organic carbon content ofsoil was significantly different between inside and outside Ampe-lodesmos tussocks in the case of large individuals, with highestvalues inside the tussocks, whereas no significant differences wereobserved in the case of small tussocks (Table 3). Soil salinity wassignificantly higher only inside large burned tussocks compared toall other tested conditions (Table 3). Soil bulk density was lowerinside large tussocks, with lowest values in post-fire conditions(Table 3). Total N and exchangeable Caþþ were highest inside largetussocks and lowest in unburned areas (Table 3). Finally, differencesof pH among all the tested conditions were not significant (Table 3).

4. Discussion

The capability of the perennial tussock grass Ampelodesmosmauritanicus to improve establishment and growth of hetero-specific showed a clear ontogenetic shift, modulated by fire occur-rence. As such, the effects of Ampelodesmos on coexisting specieswere mostly competitive in absence of fire, independent of tussocksize, then turning into facilitative for large tussocks after fire. Thefacilitative role of nurse plants rely on their ability to alter thesurrounding environment, thus enhancing the seedling recruitmentof beneficiaries (Bonanomi et al., 2011). Among the possible envi-ronmental modifications induced by large Ampelodesmos tussocksafter the fire passage, we showed both an alteration of soil quality(Table 3), a dramatic reduction of physical space limitation bystanding tillers, and changes in light attenuation through the can-opy due to tussock structure (Fig. 2), likely affecting the recruitmentof co-occurring plants. The centrifugal growth of A. mauritanicustillers and rhizomes produced, in old and large individuals, regularlyring-shaped tussocks (Fig. 1). In absence of fire, such shaping wasnon-explicitly evident even in the case of very large tussocks(diameter >1 m; Bonanomi G., pers. obs.) with dead tillers standingupright in the tussock centre area. As a consequence, a significantlight attenuation occurred along the vertical profile inside un-burned, large Ampelodesmos tussocks (Fig. 2). The extremely lowPAR values at ground level, in addition to the limited space avail-ability due to the abundance of dead standing tillers and litter

ll or large Ampelodesmos tussocks and from the outside zone. Data aremean�1 SE fors within each fire regime. Significant difference between fire regimes are in italic and

Burned areas

IN large OUT IN small IN large

7.6 � 0.3 a 7.8 � 0.2 a 7.4 � 0.3 a 7.5 � 0.8 a154 � 22 a 167 � 25 a 175 � 36 a 364 � 58 b38.3 � 5 b 27.6 � 5 a 23.6 � 6 a 33.1 � 4 b2.86 � 1.1 a 3.61 � 1.5 a 4.22 � 1.1 a 5.80 � 0.9 b21.4 � 8.6 a 30.4 � 5.9 a 28.0 � 4.5 a 39.1 � 5.2 b0.99 � 0.1 b 1.21 � 0.1 a 1.16 � 0.1 a 0.73 � 0.1 c

G. Incerti et al. / Acta Oecologica 49 (2013) 116e124122

accumulation (Fig. 2), could have likely prevented facilitative effectsby large unburned tussocks. Interestingly, a slight amelioration ofsoil quality was locally found under large unburned tussocks(Fig. 3). In such conditions beneficial effects on seedling recruitmentcould have potentially been promoted (Bonanomi et al., 2011).However, plant cover and species richness were consistently null inboth study sites (Tables 1 and 2), thus suggesting that facilitativeeffects, if any, would have been overcome by competitive effects.This is consistent with the strong competitive effects reported byArmas and Pugnaire (2011) for the tussock grass Stipa tenacissima.

After fire passage, with above-ground standing tillers removedby burning, the ring shape of Ampelodesmos became explicit due totiller resprouting from the rhizomes only at the external peripheryof the tussocks (Fig. 1). In such conditions, light attenuation in thecentral tussock area was negligible (Fig. 2), with high PAR values atground level likely producing a competitive release above groundas well. Moreover, burning produced significant changes in soilproperties (Table 3), primarily inside large Ampelodesmos tussockswith either an increase and decrease of soil salinity and bulk den-sity, respectively. After fire passage large tussocks appeared as wide“cups” filled, in the inner zone, with a deep ash layer (Fig. 1)replacing formerly standing tillers, roots and rhizomes (BonanomiG., pers. obs.), suggesting a competitive release below ground. Suchhypothesis is consistent with the findings on the ring-formingtussock Scirpus holoschoenus by Bonanomi et al. (2005) reporting,by using a non-radioactive tracer, the absence of functional rootsfrom inside the plant clones.

To our knowledge, the present study provides the first evidenceof heterospecific facilitation arising from competitive release of adominant species mediated by fire occurrence. In this way, ourresult is consistent with the findings of Vilà and Lloret (2000b),reporting that the magnitude of competitive interaction of Ampe-lodesmos with woody species was negligible after fire. However,other possible facilitation mechanisms could be putativelyconsidered in relation to our findings. Soil properties inside largetussocks were generally affected by fire occurrence (Table 3). Inparticular, the accumulation of ash into a deep inner layer produceda significant decrease of the soil bulk density, which may haveeventually promoted root growth of woody plants at the earlyregeneration stage, as also shown by Moro et al. (1997) and Pootand Lambers (2003). On the other hand, Ampelodesmos burnedtussocks were completely bare, so that PAR values at ground levelinside and outside burned tussocks were comparable. The occur-rence of the moss F. hygrometrica in such conditions confirms otherobservations of this species dominance of post-fire successionaldynamics (Esposito et al., 1999). Accordingly, heterospecific facili-tation through amelioration of micro-climatic conditions could belikely excluded. Facilitative interactions have been also related toprotection from grazing (Callaway, 2007). Given the recurrent openstructure of burned tussocks (Fig. 1), the role of Ampelodesmos inproviding protection to palatable heterospecifics should beconsidered at most as limited. However, further studies shouldspecifically address the importance of microclimate ameliorationand protection from grazing, as well as that of other possiblefacilitation mechanisms.

Despite plant facilitation potentially play a crucial role for plantcommunity organization, little attention has been paid to thespecies-specificity of this interactive process (but see Callaway,1998; Bonanomi et al., 2011). At the scale of the whole commu-nity we found that neither plant cover nor species richness arehigher inside Ampelodesmos tussock compared to the outer area.On the other hand, our results show that facilitative interactionsbetween burned Ampelodesmos tussocks and heterospecific pro-tégées are highly species-specific. In detail, we found a sharp

positive, facilitating effect on all shrub and tree species, includingseveral nitrogen fixing species. Considering the softness of the soilbed in the inner area of burned tussocks, this finding, consistent inboth study sites (Tables 1 and 2), reflects previous observations ofbeneficial effects mediated by a reduction of soil bulk-density(Moro et al., 1997; Poot and Lambers, 2003). C. monspeliensis isthe only woody species not showing the observed facilitationwithin the burned tussocks. This species is an obligate seeder, oftendominant in Mediterranean habitats degraded by recurrent fires(Roy and Sonie, 1992), being also well known for its ability toregenerate after fire by seed germination from soil seed banks, withhigh seed persistence and viability (e.g. Clemente et al., 2007). Assuch, its post-fire spreading, with seedling abundance much higheroutside than inside Ampelodesmos tussocks (Table 2), can be mostlyrelated to its well known heat stimulation requirements forgermination (Aronne and Mazzoleni, 1989; Mazzoleni, 1989), andto heterospecific competition among the seeds and seedlings ofwoody beneficiaries facilitated by Ampelodesmos inside burnedtussocks. In fact, most Cistus seeds are likely to be found in the areasoutside of Ampelodesmos tussocks, because the central burningwith ash accumulation is likely to reach temperatures which wouldkill the eventually present seeds. Different is the case of other shruband tree species that are disseminated after the fire and can find afavorable seed bed inside burnt Ampelodesmos tussocks. This is thecase of C. villosa, S. junceum, Dittrichia viscosa and Q. pubescenssubsp. pubescens whose post-fire occurrence showed a facilitationeffect in the inner area of large burned tussocks (Fig. 4). Amongherbaceous plants, two Plantago species weremuchmore abundantoutside than inside Ampelodesmos tussocks. This pattern was alsofound for other species (Tables 1 and 2), and further studies areneeded to clarify the underlying causal factors. Concerning themechanisms of plant facilitation, the above-ground competitiverelease after fire should be beneficial for all species, instead ofproducing the observed species-specific facilitation patterns. Onthis base, a specific affinity of protégé plants with the burned tus-socks can be related to the ashy substrate accumulated inside thering.

Interestingly, we found Ampelodesmos seedling recruitmentonly outside the conspecific tussocks, irrespective of their size,after fire passage. This result suggests a lack of self-facilitation(Bonanomi et al., 2010), eventually contrasting with the finding ofVilà and Lloret (2000a) reporting self-facilitation for Ampelodesmosseedling rooted outside, but under the canopy of conspecificsadults. The observed pattern might also well reflected a species-specific negative feedback on Ampelodesmos establishment by theburned residuals of the same species.

Facilitative interactions between ring-forming plants andcoexisting species that colonise the inner die-back zone have beenearly reported (Watt, 1947; Curtis and Cottam, 1950). Empiricalevidence of such interactions exists for ring-forming plants incommunities either with low productivity or affected by chronicenvironmental stress (Pedemasa, 1981; Castellanos et al., 1994;Rubio-Casal et al., 2001), and even in productive grasslands(Bonanomi et al., 2005). However, as far as we know, this is the firstcase of positive interactions by a ring-forming tussock nurse that ismodulated by plant size and fire occurrence. However, in this studyonly indirect evidence of facilitation has been reported (i.e. spatialassociations between plant species with different types of Ampe-lodesmos tussocks), while we acknowledge that such spatial pat-terns can be due, in some cases, to specific distribution of externalfactors. Further field experiments, manipulating tussock structure,are needed to prove the occurrence of Ampelodesmos facilitativeeffects and to clarify the relative importance of different facilitativemechanisms.

Fig. 4. Schematic representation of Ampelodesmos mauritanicus dynamics in unburned (above) and burned (below) stands. In absence of fire the ring shape of large tussock ishidden by the presence of standing dead tillers in the central tussock zone. After fire, ring shapes become explicit in large tussocks where resprouting is limited to the externalrhizome structures. Cistus seeds germinate after heat stimulation of soil seed bank, while ashy beds inside the Ampelodesmos rings facilitate the establishment of several otherwoody species arriving by post-fire seed dispersal (arrows).

G. Incerti et al. / Acta Oecologica 49 (2013) 116e124 123

Acknowledgements

The authors thank Silvia Caporaso, Assunta Esposito and Gian-luca Russo for technical support during field surveys.

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