Changes in plant functional types in response to goat ...

ARTICLE IN PRESS Journal of Arid Environments

Journal of Arid Environments 64 (2006) 298–322 www.elsevier.com/locate/jnlabr/yjare

Changes in plant functional types in response to goat and sheep grazing in two semi-arid shrublands of SE Spain$ T. Navarroa,, C.L. Aladosb, B. Cabezudoa a

Dpt. Biologıá Vegetal, Universidad de Ma´laga, Apd. 59, 29080 Ma´laga, Spain Instituto Pirenaico de Ecologıá, Avda, Montanãna 1005, Apd. 202, 50080. Zaragoza, Spain

b

Received 2 July 2003; received in revised form 4 October 2004; accepted 10 May 2005 Available online 1 August 2005

Abstract In Mediterranean plant communities, grazing induces severe floristic changes affecting the life histories of grazed and non-grazed species. Alteration of the grazing regimen causes important changes in the structure and dynamics of the plant community and ecosystem stability. To determine the susceptibility of different plant functional types to landscape management, we measured changes in Plant Functional Types (PFTs) in response to grazing by goat and sheep in an inland dwarf-palm matorral and a marine-exposed thorny-shrub matorral in Cabo de Gata Natural Park (SE Spain). We classified the major life forms into PFTs, and identified six PFT shrubs (dwarf-palms, sclerophyllous small trees, xeric thornyshrubs, spiny legumes, glaucous dwarf-shrubs, and xeric half-shrubs), four PFT forbs (leafy stem herbs, xeric prostrate herbs, rosette herbs, and clonal spiny herbs), and two PFT grasses (steppe and short grasses). Morphological traits measured include sclerophilly, leaf presence, leaf size, shape of leaf margins, hairiness, position of dormant buds (growth form), clonality, plant coverage, canopy structure, phenological deciduousness (drought resistance), and regeneration (reproduction type, pollination type, inflorescence position, and seed size). There was a higher correlation within and between morphological growth forms, leaf and phenological traits, than within regenerative traits (only seed size was correlated with main dispersal type). We analysed the importance of these PFTs at several sites of the two Abbreviations: PFT, Plant functional type $ For Nomenclature see: Tutin et al. (1964–1980), Castroviejo (1986/2003). Corresponding author. Tel.: +34 952 134220; fax: +34 952 131944. E-mail address: [email protected] (T. Navarro). 0140-1963/$ - see front matter r 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.jaridenv.2005.05.005

ARTICLE IN PRESS T. Navarro et al. / Journal of Arid Environments 64 (2006) 298–322

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communities, which were subjected to different livestock rates. In inland and marine-exposed communities, the same PFTs decreased in response to medium-high grazing: sclerophyllous small trees (Quercus coccifera, Olea europaea var. sylvestris), glaucous dwarf-shrubs (Phlomis and Cistus spp.) and short grasses (Brachypodium retussum). In both communities, the decrease of these grazing-susceptible PFTs was widely associated with an increase in steppe grasses (Stipa tenacissima, ‘‘alfa-grass’’) and xeric prostrate herbs (Fagonia cretica, Paronichia sufruticosa), the latter of which is a reliable indicator of degradation in semi-arid systems. Instead, different PFTs behave as either grazing-averse and/or grazing-tolerant in each community: Dwarf-palms (Chamaerops humilis) and xeric thorny shrubs (Periploca laevigata) in the marine-exposed community, and xeric half-shrubs (Thymus hiemalys, Sideritis osteoxylla, Teucrium spp., Artemisia herba-alba) in the inland community. The latter functional group resists disturbances, such as medium-moderate grazing and drought, in semiarid zones and is an indicator of long-term degradation. r 2005 Elsevier Ltd. All rights reserved. Keywords: Plant functional type; Grazing disturbance; Xeric plant trait; Semi-arid Mediterranean shrubland; Xeric half-shrub; Steppe grass

1. Introduction Ecosystem disturbance is associated with vegetation changes, such as floristic variation and vegetation regression (Connell and Slatyer, 1977; Pickett et al., 1987). Nevertheless, it is difficult to describe and analyse the dynamics of vegetation regression because communities often represent an intermediate position between two different stages (Quezel and Barbero, 1990) and the vegetation units are arbitrary products of classification, rather than natural units that are clearly defined in the field (Whittaker, 1956). Such units are merely composed of plant species that coexist at a given point in space and time. To resolve that problem, numerous approaches have been developed to study vegetation changes (Clements, 1916; Tilman, 1985; van der Maarel, 1988; Millet et al., 1998), and they lead to the conclusion that vegetation changes, such as vegetation regression, can be explained by the attributes and interactions between different species. Thus, study of the attributes of individual species is of primary importance in understanding vegetation changes and the response to disturbance. Plant Functional Types (PFTs) place a species in a group, the members of which have similar combinations of functional attributes (Solbrig, 1993) and respond similarly, or are similarly sensitive to environmental disturbance (Aguiar et al., 1996; Gitay and Noble, 1997; Lavorel et al., 1997). Functional classifications provide a framework for describing vegetation changes in natural ecosystems in terms of functional traits as a response to disturbance (Grime et al., 1997) and grazing in Mediterranean ecosystems (Fernańdez-Ale´s et al., 1993; Hadar et al., 1999; Diaz et al., 2001). Additionally, they provide predictive models of vegetation dynamics and vegetation changes (Box, 1996; Skarpe, 1996; Lavorel et al., 1997; McIntyre et al., 1999b; Diaz et al., 2002) and reduce the complexity of species diversity to a few key plant types, which helps to predict the composition and functioning of ecosystems in

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T. Navarro et al. / Journal of Arid Environments 64 (2006) 298–322

a changing environment (Woodward and Cramer, 1996). PFTs are used to evaluate ecosystem dynamics (Noble and Gitay, 1996), and can provide information on ecological adaptations and survival mechanisms in extreme environments (Weiher et al., 1999; Jauffret and Lavorel, 2003). In arid Mediterranean ecosystems, climate variation and grazing are the main factors affecting degradation processes through long-term changes or loss of vegetation (Le Houe´rou, 1981, 2001; DiCastri et al., 1981; Milchunas et al., 1988; Diaz Barradas et al., 1999; Jauffret and Lavorel, 2003). In semi-arid regions, such as Cabo de Gata (SE Spain), grazing is responsible for certain changes in the natural vegetation, where the seral thyme brushwood (Thymus spp.) and alfa-grass (Stipa tenacissima) finally develop (Alados et al., 2003). Communities of alfa-grass develops after the degradation of open dry forests (Le Houe´rou, 1959, 1969; Merce´, 1989) and occupy important areas in the arid Mediterranean region (Le Houe´rou, 1986), particularly in SE Spain (Gauquelin et al., 1996; Cerda´, 1997) and, under intensive grazing, perennial bunch-grasses also disappear (Noy-Meir, 1990; Bisigato and Bertiller, 1997). Seral thyme brushwood occurs in regions subjected to intensive grazing (Tomaselli, 1981) and they are the predominant vegetation in many Mediterranean areas (Ozenda, 1975), including Cabo de Gata (Peinado et al., 1992). To investigate the use of PFTs as indicators of long-term floristic vegetation changes in response to grazing in the semi-arid shrubland ecosystems, we compared two communities in Cabo de Gata Natural Park that differ in the degree of exposure to a marine environment along a grazing disturbance gradient. We asked the following questions: 1. Can functional types be identified among the major life forms (shrubs, forbs, and grasses)? 2. What are the relevant traits that define the different functional types in the semiarid shrublands? 3. Does the response of PFTs to grazing differ between the inland and marine coastal communities? 4. What is the ecological significance of the functional response in semi-arid communities? To answer those questions, we recorded morphological, phenological, and regenerative traits (McIntyre et al., 1999a, b; Cornelissen et al., 2003) and classified those traits using multivariate statistical techniques (Leishman and Westoby, 1992; Golluscio and Sala, 1993).

2. Materials and methods 2.1. Study site Cabo de Gata Natural Park is on the southeast coast of Spain in a volcanic mountain range at 493 m asl. Soil erosion is high, and reaches values of


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50–100 t ha1 year1 of soil lost (Oyonarte et al., 1999). The climate is Mediterranean semi-arid, characterized by mild summer temperatures, and an average annual rainfall of 193.9 mm (between 1973 and 1996, at 43 m asl). The mean annual temperature is 19.4 1C (Passera, 1999). The study was conducted at a mid-slope position, which is representative of the natural rangeland vegetation of the area. We avoided sampling summits because of their high degree of rockiness and variable slopes, which would have interfered with the homogeneity of the sites surveyed. We studied two ecological communities within a semi-arid ecosystem: (1) a dense matorral of thorny-bushes (Periploca laevigata), (Freitag, 1971; Peinado et al., 1992), which is a typical arid vegetation in marine-exposed areas that have mild temperatures in summer, and (2) a moderately dense matorral of dwarf-palms (Chamaerops humilis) with Ulex baeticus and Rhamnus lycioides (Peinado et al., 1992), which are typical dry and thermic vegetation found in inland areas, where there is a stronger continental influence on. The composition of plant assemblages varies among ecosystem types (McIntyre et al., 1999a). In our study area, perennial grasses and perennial and short-lived forbs are represented by only a few species, while shrubs (dwarf and half-shrubs) represent 65% of the species in the inland communities and 47% in the marine coastal communities. We focused our analysis on woody plants and short-lived and perennial herbs. With 25 species from 13 families, the inland matorral of dwarf-palms was the richest community. The coastal matorral of thorny-bushes comprised 22 species in 11 families. The most abundant and widespread families were Lamiaceae, which was represented by nine dwarf and half-shrub species, and Gramineae and Fabaceae, which were represented by three and two species, respectively. Fagaceae, Oleaceae, Aracaceae, Rhamnaceae, and Asclepiadaceae represented the evergreen and sclerophyllous species, and Zygophyllaceae comprised the most xeric floristic elements. Four grazing pressures (mixed herds of sheep and goats) were evaluated in the marine coastal matorral: Corn1 (ungrazed), Corn2 (0.27 individual ha1 (ind. ha1)), Corn3 (0.46 ind. ha1), and Corn4 (0.65 ind. ha1). In the inland matorral, six grazing pressures were evaluated: Palm1 (0.24 ind. ha1), Palm2 (0.40 ind. ha1), Palm3 (0.56 ind. ha1), Palm4 (1.09 ind. ha1), Palm5 (1.82 ind. ha1), and Palm6 (2.58 ind. ha1). To calculate the effective stocking rate of each farm, we multiplied the average stocking rate of the farm (ind. ha1) by the proportion of the land used for grazing, which we obtained from direct observation (animals were followed one week per season) of the proportion of time that each grazing site was used. Each grazing site considered covered approximately 30 ha. We collected data using a Global Position System (GPS) and transferred to a digitized map in Geographical Information System (GIS) format. The effect of grazing on vegetation includes defoliation, trampling, and defecation. Consequently, in this study, we use the term tolerance to grazing with reference to the overall effect of grazing, which includes both the plant response to defoliation and the effect of soil degradation.



2.2. Vegetation sampling From 15 to 30 April 2001, we surveyed the vegetation by randomly selecting 30 line-intercept transects that were 500 m in length (3 per grazing treatment). Transects were located horizontally along the mid-slope position. The abundance of a species was estimated by the frequency of its occurrence at 20-cm intervals along each transect. To better understand landscape-level successional changes, our analyses focused on dominant perennial and short-lived species that have biogeographical significance and had relative abundances of 41%. 2.3. Plant traits To explore the existence of functional types within the major life forms, we classified each species based on their growth form and life-cycle (Lavorel et al., 1997; McIntyre et al., 1999a, b), which yielded three groups (shrubs, forbs, and grasses). Forbs included short-lived and perennial herbs, grasses included perennial grasses, only, and shrubs included woody plants 0.5–5 m high. Those groups provide the possibility of describing natural correlations between traits and investigating different sets of traits among life forms (Lavorel et al., 1997, 1999). For each species, we collected morphological, phenological, and regenerative data (Appendix) in the field. When field specimens were inadequate, we used herbarium specimens. Shrub morphology was described by plant coverage (PLCO), position of dormant buds (based on Raunkiaer growth forms) (DOBU), stem morphology (related to plant architecture) (STMO). Leaf phenology (deciduousness) (DEDU), which reflects the degree of drought resistance and the plant’s response to aridity, is a relevant trait of shrubs (McIntyre et al., 1999a), particularly in arid ecosystems. Clonality (CLONA) is associated with climate, disturbance, and responses to soil resources (Cornelissen et al., 2003). Spininess or thorniness (SPNY) is associated with defence against herbivores and climate (Cornelissen et al., 2003), leaf size (Westoby, 1998), and leaf consistency (sclerophilly) (LECO), both of which are correlated (Turner, 1994) and associated with disturbance regimes and climate. Hairiness (trichomes) (HAIR), which is associated with drought tolerance (Keshet et al., 1990), leaf colour (both sides) (LELO), leaf presence (connected to green stems) (LEPR), and the shape of leaf margins (REVO) were included. Regeneration traits were described by type of reproduction (sexual or asexual) (RETY), the latter of which is associated with clonality in perennials, pollination type (POTY), seed size (SESI), inflorescence position (INPO), and main dispersal type (DITY) are strongly associated with disturbance (Cornelissen et al., 2003). Forb morphology was described using life-cycle (LIFE), canopy structure (CAST), height (HEIG), which are characteristics associated with grazing (Jauffret and Lavorel, 2003), plant coverage (PLCO), spininess (SPNY), stem morphology (STMO), lateral spread (LASP) (important attribute that characterize plant shape, and space occupancy, McIntyre et al. (1999a)). Lateral spread is a relevant trait in open matorrals, and height is closely related to the response to disturbance


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(Diaz et al., 1992). Regenerative traits included inflorescence position (INPO), pollination type (POTY), and main dispersal type (DITY). The traits of grasses were described using plant coverage (PLCO), canopy structure (CAST), leaf consistency (LECO), height (HEIG), seed size (SESI), and inflorescence position (INPO). 2.4. Data analyses 2.4.1. Classification of the major life forms into PFTS To explore the existence of PFTs within the major life-forms (shrubs, forbs and grasses), and to characterize the responses to specific disturbances in a given vegetation type, classification should operate in an explicitly hierarchical manner (Golluscio and Sala, 1993; Lavorel et al., 1997; McIntyre et al., 1999b). To obtain a dendrogram that illustrated the potential clusters, we used a sequential, agglomerative, hierarchical clustering analysis that involved a complete linkage method (Wilkinson et al., 1992). We constructed a set of traits: 17 traits 20 shrub species, 15 traits 5 forb species, and 7 traits 3 grass species, and calculated the similarity matrix based on the w2 index. That classification is non-subjective in its grouping of species within functional types. In each case, the species clusters were assumed to represent PFTs at the species level. Such hierarchical techniques are often used for cluster analyses of biological data (Everitt, 1974; Podani, 1989). Statistical analyses were performed using SPSS 12.0 software. To determine the relative importance of each trait in determining different PFTs, we performed Principal Components Analysis (PCA) on untransformed trait values and used correlation coefficients as a measure of similarity between species (Orloći, 1978). The location of a species on the different PCA axes results from a different linear combination of the values of the attributes (traits). The importance of a trait on one axis is proportional to its coefficient in the linear combination defining the axis. Additionally, we evaluated the association among traits using the Kendall rank correlation (Sokal and Rohlf, 1995). 2.4.2. Characterization of the response of PFTs to grazing We used least-squared regression to analyse the response of each PFT to grazing disturbance. Abundances were based on relative frequency and subjected to angular transformation (Sokal and Rohlf, 1995). Statistical analyses were performed using SPSS 12.0 and SAS V8 software.

3. Results 3.1. Classification of PFTs and trait assessments We identified three major functional types of shrubs: evergreen small trees and large shrubs (trees/shrubs 1–5 m) (PFT 1), evergreen large spiny shrub legumes (PFT 2), and deciduous pioneer dwarf and half-shrubs (shrubs 0.5–0.80 m) (PFT 3). PFT 1 was divided into sclerophyllous dwarf-palms large leaves (PFT 1.1),



sclerophyllous small trees (PFT 1.2), and xeric thorny-shrubs (PFT 1.3). PFT 3 was divided into glaucous dwarf-shrubs (PFT 3.1) and xeric half-shrubs (PFT 3.2), (Fig. 1). The most important attributes that differentiated shrub functional types were deciduousness (DEDU), pollination type (POTY), spininess or thorniness (SPNY), inflorescence position (INPO), clonality (CLONA), reproduction type (RETY), leaf consistency (LECO), leaf presence (LEPR), position of dormant buds (DOBU), stem morphology (STMO), leaf margins (REVO), leaf size (LESI), hairiness (HAIR) and seed size (SESI). The first PCA axis accounted for 76% of the variance and had high positive loading with RETY, SPNY, INPO, and CLONA, and high negative loading with DEDU, LECO, POTY, STMO, LEPR and DOBU (Table 1). Pioneer dwarf and half-shrubs (PFT 3) were at one extreme because they are deciduous, nonsclerophyllous and enthomophyllous dwarf and half-shrubs with exposed inflorescences and without spines. At the other extreme were the evergreen small trees and large shrubs: the spiny and aphyllous legumes (PFT 2), the xeric thorny-shrubs (PFT 1.3), the sclerophyllous dwarf-palms (PFT 1.1), and the sclerophyllous and anemophyllous small trees (PFT 1.2) (Fig. 2a). The second axis accounted for 13% of the variance and had high positive loading with leaf margins (REVO), leaf size (LESI), hairiness (HAIR), and seed size (SESI) (Table 1). Spiny legumes (PFT 2) was clearly differentiated because it is the only group without leaves. Glaucous dwarf-shrubs (PFT 3.1) with medium and non-revolute leaves and glaucous indumentum was distinguished from xeric half-shrubs (PFT 3.2) without glaucous indumentum and small revolute leaves. (Fig. 2a). The third axis accounted for 6% of the variance. Hairiness (HAIR) had significant positive loading and leaf size (LESI) negative. (Table 1). Dwarf-palms (PFT 1.1) was at one extreme because it has large leaves and xeric half-shrubs ( PFT 3.2) differed from the others because it is a group that has small leaves (Fig. 2b). Sclerophilly (LECO) and deciduousness (DEDU) were significantly positively correlated with renewal bud location (DOBU) (t ¼ 0:78; po0:01). In turn, those attributes were significantly negatively correlated with plant coverage (PLCO) (t ¼ 0:89; po0:01), seed size (SESI) (t ¼ 0:89; po0:01) and dispersal type (DITY) (t ¼ 0:78; po0:01). Evergreen sclerophyllous species (PFT 1) are phanerophytes that have large coverage, medium-sized seeds, and dispersal by agents other than wind. The deciduous species with non-sclerophyll leaves are dwarf or half-shrubs (PFT 3), which have small coverage and dispersal by the wind. Inflorescence position (INPO) was highly positively correlated with plant coverage (PLCO) (t ¼ 0:7; po0:01). Species that have exposed inflorescences have small coverages (PFT 3). We identified four functional types of forbs: perennial clonal spiny herbs (PFT 1), short-lived rosette herbs (PFT 2), short-lived leafy stem herbs (PFT 3), and shortlived xeric prostrate herbs (PFT 4) (Fig. 1). The major attributes that differentiated forb functional types were seed size (SESI), plant coverage (PLCO), life-cycle (LIFE), leaf presence (LEPR), clonality (CLONA), reproduction type (RETY), stem morphology (STMO), inflorescence position (INPO), canopy structure (CAST), and hairiness (HAIR) (Table 1). The first PCA axis accounted for 67% of the variance,


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Fig. 1. Classification of major life forms (shrubs, forbs, and grasses) using cluster analysis, which include 26 woody plants, small trees and large shrubs, dwarf and half-shrubs, perennial and short-lived herbs, and perennial grasses of Cabo de Gata Natural Park.



Table 1 Component matrix (factor loadings) contribution to the first axes of the Principal Component Analysis Axe 1

Axe 2

Axe 3

Shrub traits PLCO RETY LESI DEDU LECO LELO HAIR SPNY POTY CLONA SESI STMO LEPR INPO REVO DOBU DITY

0.894 0.940* 0.350 0.958* 0.941* 0.783 0.700 0.952* 0.957* 0.940* 0.894 0.906* 0.936* 0.968* 0.683 0.904* 0.927

0.433 0.261 0.627* 0.199 0.238 0.369 0.479* 0.057 0.103 0.261 0.433* 0.315 0.300 0.040 0.681* 0.419 0.258

0.081 0.160 0.667* 0.023 0.192 0.026 0.499* 0.215 0.223 0.160 0.081 0.222 0.143 0.164 0.167 0.051 0.229

Forb traits CAST SESI PLCO LIFE SPNY POTY RETY STMO LEPR HAIR INPO LASP HEIG CLONA DITY

0.419 0.994* 0.994* 0.994* 0.859 0.567 0.994* 0.451 0.994* 0.419 0.451 0.872 0.872 0.994* 0.859

0.820* 0.036 0.036 0.036 0.463 0.477 0.036 0.852* 0.036 0.820* 0.852* 0.473 0.473 0.036 0.463

The most important shrub and forb attributes, for each component, are highlighted by an asterisk.

had four attributes with high negative loading (PLCO, LIFE, LEPR, and CLONA), and two attributes (SESI) and (RETY) with high positive loading. Perennial herbs were clearly differentiated because they are the only perennial clonal group with high coverage, medium-sized seeds, and without leaves (Fig. 2c). The second axis accounted for 26% of the variance and had four attributes with positive loading (CAST, STMO, HAIR, and INPO) (Table 1). Leafy stem herbs were at one extreme because they have simultaneously erect hairy stems and exposed inflorescences. At the other extreme were the xeric herbs that have prostrate stems


1.0

0.6

QC

OE

Glaucous dwarf-

Dwarf-palms PFT 1.1 Xeric thorny-shrubs RL PFT 1.3 PL

shrubs PFT 3.1

AXIS 2

CH

0.0

LS CA

PH PS PP AH TC TH SO Xeric half-shrubs PFT 3.2

Spiny legumes PFT 2

-0.5

DG

0.3

UP

-0.5

0.0

0.5

TH

-0.5

0.0

SO

CS CA Glaucous dwarf- LS TL shrubs PFT3.1 TC PS PP

CH Dwarf-palms PFT 1.1

-1.0

1.0

AXIS 1

Sclerophyllous trees PFT 1.2 QC

OE

-1.0

-1.0

Xeric half-shrubs PFT 3.2 AH

GU

Spiny legumes PFT 2

0.2

0.0 GU

-1.0

0.4

0.1

UP

(a)

PL Xeric thorny-shrubs PFT 1.3 RL

0.5

Sclerophyllous trees PFT 1.2

AXIS 3

DG

0.5

307

PH

0.5

1.0

AXIS 1

(b) FC Xeric prostrate herbs PFT 4

0.5 AXE 2

PA AH

Clonal spiny herbs PFT 1

0.0 Rostte herbs PFT 2

-0.5

PS

Leafy stems herbs PFT 3 LM

-1.0 (c)

-0.5

0.0

0.5

1.0

AXE 1

Fig. 2. Location of the shrub and forb species of Cabo de Gata Natural Park along the first axes of the Principal Components Analysis. (a–b) Shrub species: SO Sideritis osteoxylla; TH Thymus hyemalis; AH Artemisia herba-alba; TC Teucrium charidemi; TL T. lusitanicum; CA Cistus albidus; CS C. salvifolius; BH Ballota hirsuta; LS Lavandula stoechas; PS Phagnalum saxatile; PP Phlomis purpurea; PH Ph. lychnitis; UP Ulex baeticus; GU Genista umbellata; RL Rhamnus lycioides; PL Periploca laevigata; QC Quercus coccifera; OE Olea europaea; DG Daphne gnidium; CH Chamaerops humilis. (c) Forb species: PA Paronichia sufruticosa; FC Fagonia cretica; LM Lavandula multifida; PS Plantago albicans; AH Asparragus horridus.

without hairs and with protected inflorescences (Fig. 2c). Plant coverage (PLCO) was highly positively correlated with life cycle (LIFE), leaf presence (LEPR), and clonality (CLONA) (t ¼ 1; po0:05), and negatively correlated with seed size (SESI) (t ¼ 1; po0:05). Perennial herbs are clonal plants that have high coverage and medium-sized seeds. The short-lived herbs have small coverages and small seeds. We identified two major functional types of perennial grasses: short grasses (PFT 1), including summer semi-deciduous grasses and steppe grasses (PFT 2), including tussock perennial species, with large canopies, semi-sclerophyllous and narrow leaves (Fig. 1).



3.2. Variations in the response of PFTs to grazing Our comparison of the proportions of different functional groups in each of the two communities (Figs. 3 and 4) revealed that there were significantly more xeric thorny-shrubs (PFT 1.3), short-lived leafy stem herbs (PFT 3), and steppe grasses (PFT 2) in the marine coastal community, and significantly more large spiny shrub legumes (PFT 2), xeric half-shrubs (PFT 3.2), glaucous dwarf-shrubs (PFT 3.1), xeric prostrate herbs (PFT 4) and short grasses (PFT 1) in the inland community. When we compared the variation of each PFT abundance across grazing intensities, we identified three main groups of species: grazing-sensitive species (or grazing decreasers), grazing-tolerant species (those that remain unchanged), and grazing-favoured species (or grazing increasers). The abundance of dwarf-palms, glaucous dwarf-shrubs, and short grasses were significantly negatively correlated with grazing pressure (Table 2). In both communities, the decrease in those grazing-sensitive PFTs was associated with a significant increase in the abundance of xeric prostrate herbs. In the inland community (Fig. 3), the most grazing-sensitive shrub species included dwarf-palms (PFT 1.1) (slope ¼ 0.17, R2 ¼ 0:70, F 1;16 ¼ 35:45, po0:001), sclerophyllous trees (PFT 1.2) (slope ¼ 0.035, R2 ¼ 0:59, F 1;16 ¼ 23:31, po0:001), spiny legumes (PFT 2) (slope ¼ 0.065, R2 ¼ 0:76, F 1;16 ¼ 51:50, po0:001), glaucous dwarf-shrubs (PFT 3.1) (slope ¼ 0.115, R2 ¼ 0:86, F 1;16 ¼ 100:77, po0:001), and short grasses (PFT 1) (slope ¼ 0.216, R2 ¼ 0:79, F 1;16 ¼ 61:02, po0:001) and, at a lower intensity, the xeric thorny-shrubs (PFT 1.3) (slope ¼ 0.028, R2 ¼ 0:50, F 1;16 ¼ 15:73, po0:001). The grazing-tolerant shrub species included the xeric half-shrubs (PFT 3.2) (R2 ¼ 0:16, F 1;16 ¼ 3:00, NS) and, among the forbs, the rosette herbs (PFT 2) (R2 ¼ 0, F 1;16 ¼ 0:01, NS). Grazing increasers included xeric prostrate herbs (PFT 4) (slope ¼ 0.037, R2 ¼ 0:48, F 1;16 ¼ 12:68, po0:01), leafy stem herbs (PFT 3) (slope ¼ 0.045, R2 ¼ 0:78, F 1;16 ¼ 55:83, po0:001), clonal spiny herbs (PFT 1) (slope ¼ 0.016, R2 ¼ 0:30, F 1;16 ¼ 6:72, po0:05), and steppe grasses (PFT 2) (slope ¼ 0.210, R2 ¼ 0:89, F 1;16 ¼ 128:63, po0:001). In the marine coastal community (Fig. 4), the grazing-sensitive shrub species included the xeric half-shrubs (PFT 3.2) (slope ¼ 0.307, R2 ¼ 0:75, F 1;10 ¼ 30:16, po0:001), glaucous dwarf-shrubs (PFT 3.1) (slope ¼ 0.121, R2 ¼ 0:41, F 1;10 ¼ 6:84, po0:05); among the forbs, leafy stem herbs (PFT 3) (slope ¼ 0.181, R2 ¼ 0:59, F 1;10 ¼ 14:19, po0:001) and shorts grasses (PFT 1) (slope ¼ 0.307, R2 ¼ 0:78, F 1;10 ¼ 34:83, po0:001). Grazing-tolerant shrub species included the dwarf-palms (PFT 1.1) (R2 ¼ 0:01, F 1;10 ¼ 0:09, NS), xeric thorny-shrubs (PFT 1.3) (R2 ¼ 0:12, F 1;10 ¼ 1:37, NS) and, among the forbs, rosette herbs (PFT 2) (R2 ¼ 0:11, F 1;10 ¼ 1:19, NS) and clonal spiny herbs (PFT 1) (R2 ¼ 0:30, F 1;10 ¼ 4:26, NS). The abundance of xeric prostrate herbs (PFT 4) (slope ¼ 0.056, R2 ¼ 0:37, F 1;10 ¼ 5:95, po0:05) and steppe grasses (PFT 2) (slope ¼ 0.484, R2 ¼ 0:83, F 1;10 ¼ 48:25, po0:001) were positively correlated with grazing pressure. In the inland community, the attributes associated mainly with grazing-sensitive shrub species were deciduousness (DEDU), pollination type (POTY), spininess or


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thorniness (SPNY), inflorescence position (INPO), leaf consistency (LECO), leaf presence (LEPR), position of dormant buds (DOBU), leaf margins (REVO), leaf size (LESI), hairiness (HAIR), and seed size (SESI). Medium to heavily grazed sites were characterized by an increase in dwarf or half-shrub species with revolute (REVO), small (LESI) and deciduous leaves (DOBU), and with small seed (SESI), and dispersal by the wind (DITY) (anemochores). Those attributes would reflect the responses of xeric half-shrub species of the seral thyme brushwood found in the inland community in areas of medium grazing pressure. Examples of those species include mainly Lamiaceae—Thymus hiemalys, Sideritis osteoxylla, and Teucrium spp. Grazing-tolerant forb species were associated mainly with life-cycle (LIFE), stem morphology (STMO), inflorescence position (INPO), plant coverage (PLCO), canopy structure (CAST) and hairiness (HAIR). The attributes associated with grazing-sensitive shrub species in the marine coastal community were deciduousness (DEDU), leaf consistency (LECO), position of dormant buds (DOBU), leaf margins (REVO), leaf size (LESI), hairiness (HAIR) and seed size (SESI). Grazing-tolerant forb species were mainly associated with lifecycle (LIFE), clonality (CLONA), stem morphology (STMO), and inflorescence position (INPO). Grazing-tolerant species subjected to light to moderate grazing in the inland communities were associated with the response of short grasses, whereas tolerance to medium to heavy grazing was associated with the colonization response of steppe grasses.

4. Discussion 4.1. PFTs and their attributes In this study we classified 26 species characteristics of a semi-arid, disturbed Mediterranean ecosystem into nine major PFTs based on the relevant trait response to grazing disturbance in arid zones (Diaz et al., 2002; Jauffret and Lavorel, 2003; Rusch et al., 2003; Cornelissen et al., 2003). Our results support the main Mediterranean functional classifications: the ‘‘maquis’’ species (typical sclerophyllous, evergreen plants) and the ‘‘tomillar’’ species (mallacophyllous, deciduous plants) (Orsahn, 1964; Margaris, 1981; Orshan, 1989; Terradas, 1991; Herrera, 1984, 1992; Navarro and Cabezudo, 1998; Pausas, 1999; Diaz Barradas et al., 1999). Four

Fig. 3. Relative frequency variation in relation to grazing intensity in an inland matorral of dwarf-palms of Cabo de Gata Natural Park. Palm1 ¼ 0.24 ind. ha1, Palm2 ¼ 0.40 ind. ha1, Palm3 ¼ 0.56 ind. ha1, Palm5 ¼ 1.82 ind. ha1, and Palm6 ¼ 2.58 ind. ha1. Shrub PFTs: Palm4 ¼ 1.09 ind. ha1, PFT1.1 ¼ dwarf-palms, PFT 1.2 ¼ sclerophyllous trees, PFT1.3 ¼ xeric thorny-shrubs, PFT2 ¼ spiny legumes, PFT3.1 ¼ glaucous dwarf-shrubs, PFT3.2 ¼ xeric half-shrubs. Forb PFTs: PFT1 ¼ clonal spiny herbs, PFT2 ¼ rosette herbs, PFT3 ¼ leafy stem herbs, PFT4 ¼ xeric prostrate herbs. Grass PFTs: PFT1 ¼ short grasses, PFT2 ¼ steppe grasses.


311



Table 2 Least squared regression analyses to determine the response of each PFT to grazing disturbance PFTs

Intercept

Slope

R2

F

P

Dwarf-palms Sclerophyllous trees Xeric thorny-shrubs Spiny legumes Glaucous dwarf-shrubs Xeric half-shrubs Clonal spiny herbs Rosette herbs Leafy stems herbs Xeric prostrate herbs Short grasses Steppe grasses

0.401 0.059 0.201 0.167 0.233 0.293 0.067 0.012 0.065 0.042 0.304 0.522

0.150 0.024 0.086 0.007 0.073 0.024 0.005 0.002 0.007 0.030 0.128 0.087

0.647 0.219 0.298 0.003 0.403 0.034 0.013 0.001 0.009 0.375 0.346 0.103

51.26 7.87 11.9 0.08 18.93 0.98 0.38 0.27 0.27 16.84 14.81 3.22

0.01 n.s. o 0.001 n.s. n.s. o0.001 0.01 o0.001 n.s. n.s. 0.1 o0.001

(n.s.) ¼ non-significant results. Abundances were subjected to angular transformation.

of the species groups correspond to the major functional groups that have been recognized in Mediterranean shrubland. Evergreen sclerophyllous small trees and large shrubs correspond to PFT C of Diaz Barradas et al. (1999) and to the evergreen broad-leaves Ni (2001). Large shrub legumes correspond to the PFT F and glaucous dwarf-shrubs to the PFT E of Diaz Barradas et al. (1999). Steppe grasses were referred to as cool-steppe grasses by Ni (2001), as perennial grasses with narrow leaves by Skarpe (1996). The major traits associated with this classification are drought resistance, sclerophilly, leaf presence, leaf size, leaf margins (flat or revolute leaves), hairiness, dormant bud position (growth-form), clonality, plant coverage, canopy structure, reproduction type, pollination type, inflorescence position, and seed size. There was a higher correlation within and between morphological traits; growth-form, leaf morphology (consistency, size, and revolute margins), and phenological traits (drought resistance) than within regenerative traits, in which only seed size is associated with main dispersal type, according to Grime et al. (1988) and Leishman and Westoby (1992). Clonality is the only morphological trait related to vegetative regeneration associated with plant coverage and life-cycle.

Fig. 4. Relative frequency variation in relation to grazing intensity in a marine-exposed matorral of thorny-shrubs of Cabo de Gata Natural Park. Corn1 ¼ ungrazed, Corn2 ¼ 0.27 ind. ha1, Corn3 ¼ 0.46 ind. ha1, Corn4 ¼ 0.65 ind. ha1. Shrub PFTs: PFT1.1 ¼ dwarf-palms, PFT 1.2 ¼ sclerophyllous trees, PFT1.3 ¼ xeric thorny-shrubs, PFT2 ¼ spiny legumes, PFT3.1 ¼ glaucous dwarf-shrubs, PFT3.2 ¼ xeric half-shrubs. Forb PFTs: PFT1 ¼ clonal spiny herbs, PFT2 ¼ rosette herbs, PFT3 ¼ leafy stem herbs, PFT4 ¼ xeric prostrate herbs. Grass PFTs: PFT1 ¼ short grasses, PFT2 ¼ steppe grasses.


313

Positive correlations between sclerophilly, drought resistance, and renewal bud location was reported by Montenegro et al. (1979) and Golluscio and Sala (1993) and might be related to xerophytic adaptation on rocky slopes (Diaz Barradas et al., 1999) and dry grazing communities (Grime, 1979). In Cabo de Gata and other semi-arid systems, water deficit is associated with dry and hot summers (Nobel, 1989); therefore, buds of dwarf and xeric half-shrubs remain inactive over the summer and an absolute or partial seasonal reduction in mallacophyllous leaves occurs (Zohary and Orshan, 1956; Orshan and Zand, 1962; Orsahn, 1964; Navarro and Cabezudo, 1998). 4.2. Variations in the response of PFTs to grazing In our study, as elsewhere (Bisigato and Bertiller, 1997; Jauffret and Lavorel, 2003), the abundance of glaucous dwarf-shrubs decrease with an increase grazing pressure. Similarly, dwarf-palms (Ch. humilis) were less abundant in the heavily grazed sites. Indeed, sclerophyllous trees (Quercus coccifera, Olea europaea var. silvestrys) are sensitive to grazing pressure. The response of PFT shrubs could be used to understand the mechanisms underlying community dynamics in response to grazing in arid systems. Previous studies reported a negative effect of grazing on the spatial organization of sensitive species compared to more tolerant species (Alados et al., 2003). The decrease in or elimination of grazing-sensitive groups of species was compensated by the increased development of species favoured by grazing, which induced vegetation changes by means of the colonizing process. In our study, in both communities, the decrease in grazing-sensitive PFTs subjected to heavy grazing was associated with an increase in the abundance of the perennial steppe grass S. tenacissima, which uses the water available in bare soil patches in late spring as a life-history strategy in semi-arid systems (Golluscio and Sala, 1993; Kleyer, 1999). Other studies have reported that grazing can prevent the recruitment of woody plants and transform woodlands into grasslands (Chesterfield and Parsons, 1985; Gibson and Kirkpatrick, 1989; Williams, 1990). In the inland community, glaucous dwarf-shrubs with haired, mallacophyllous and non-revolute leaves, such as Cistus or Phlomis spp., were strongly affected by grazing. Xeric half-shrubs (T. hiemalys, S. osteoxylla, Teucrium spp., Artemisia herba-alba) were not strongly affected by grazing and they comprised a grazingtolerant group, mainly in the inland community. Others have observed that xeric half-shrubs is a grazing-tolerant PFT, especially when they have a history of light grazing (Pickup and Stafford Smith, 1993; Schlesinger et al., 1996; Skarpe, 2000; Jauffret and Lavorel, 2003). The xeric half-shrubs are summer deciduous species with small, revolute and mallacophyllous leaves, often with hairs, anemochores with small seeds and flowers grouped in exposed inflorescences, such as Thymus, Sideritis and Teucrium spp., which are characteristic of the seral thyme brushwood of Cabo de Gata (Peinado et al., 1992). This group agree with the PFTs previously identified in the Mediterranean shrubland ecosystems of S Spain based on flower, seed, and leaf characteristics



(Herrera, 1984, 1992; Diaz Barradas et al., 1999), and forms part of the typical species that have evolved in Mediterranean climates and are adapted to the stress of cold and drought (Orshan, 1964, 1989; Herrera, 1984; Cabezudo et al., 1992; Correia and Catarino, 1994; Navarro and Cabezudo, 1998; Diaz Barradas et al., 1999). Xeric half-shrubs have small leaves as an adaptation to the constraints experienced in arid zones, such as grazing and drought (Milchunas et al., 1988; Briske and Richards, 1995; Jauffret and Lavorel, 2003), and they grow on poorly developed soils that are without an upper horizon and have shallow roots (Herrera, 1986). They have an aerial diaspore bank (Zohary, 1937) and flower in large populations, especially Thymus and Teucrium (Dafni and O’Toole, 1994; Navarro and El Oualidi, 1999). Grazing also favoured xeric prostrate herbs, such as Fagonia cretica and Paronichia sufruticosa, as was observed elsewhere (Grime, 1979; Tilman, 1988; Noy-Meir et al., 1989; Fernańdez-Ale´s et al., 1993; McIntyre et al., 1995; Lavorel et al., 1998, 1999; Kleyer, 1999). Ch. humilis, which tolerates a moderate level of grazing, plays an important role in the preservation of plant diversity because its large canopy and large evergreen sclerophyllous leaves help alleviate thermal and water stress more than do plants that have a small canopy (Muller, 1953; Turner et al., 1966; Fowler, 1986). The spatial distribution of Ch. humilis reflects its capacity to persist along the grazing disturbance gradient of our study area on marine-exposed slopes, maintaining the low, discontinuous matorral and retarding the transition to scattered matorral or grassland (Alados et al., 2003). Where grazing disturbance is very intense, the decreased and scattered distribution of Ch. humilis favoured encroachment by grazing-tolerant species, such as steppe grasses. It is widely accepted that species adapt to disturbance to the point that a lack of disturbance can become a disturbance in itself. In environments with a long history of grazing, such as the Mediterranean ecosystem, grazing is essential to the maintanance of species diversity (Grime, 1979; McNaughton, 1985; Milchunas et al., 1988). Moderate grazing has a positive effect on plant fitness (McNaughton, 1977, 1979, 1983; Collins, 1987; Esco´s et al., 1997; Alados et al., 1998), although an excess or a lack of grazing might be important agents of perturbation. In the marine coastal community, with a reduced level of grazing, particularly, we observed, that the wellrepresented xeric thorny-shrubs (Rhamnus and Periploca spp.) had a higher relative frequency at intermediate levels of grazing. That finding is similar to those in previous studies, which examined the effect of grazing on the stress of Periploca, and reported lower levels of stress under moderate grazing than under low or heavy grazing (Alados et al., 2002). 4.3. Indicators To gain a better understanding of the natural processes in semi-arid systems, which are necessary for the management of these systems (Wiegand and Florian, 2000), our fourth objective was to identify the indicators of the vegetation degradation using measurable attributes. Climate variability and grazing history


315

are the driving forces affecting landscape preservation in rangeland semi-arid ecosystems, which are concentrated on marginal areas where grassland production is relatively low. Previous studies demonstrated that some species are more resistant to changes in grazing pressure than are others. For example, S. tenacissima (alfa-grass steppe) is an indicator associated with grazing and supports the concept that ‘‘large, erect, grass that branches above-ground tussocks’’ is a PFT that is a potential indicator of grazing (Noy-Meir et al., 1989; Landsberg et al., 1999; McIntyre et al., 1995; Hadar et al., 1999; Skarpe, 2000; Jauffret and Lavorel, 2003; Alados et al., 2003). Half-shrubs (small to medium chamaephytes), summer deciduous with small mallacophyllous leaves and small anemochores seeds (Thymus, Teucrium, Sideritis spp., and A. herba-alba) are associated with moderate grazing pressure in the disturbed seral thyme brushwood of SE Spain and are indicators of long-term degradation that resist disturbances and reflect the degradation of vegetation cover and soils (van de Koppel and Rietkerk, 2000; Jauffret and Lavorel, 2003). Under decreased grazing pressure, PFTs can favour long-term natural restoration (Jauffret and Lavorel, 2003). Short-lived herbs, small stature, and prostrate habit are common indicators of heavy grazing and disturbance (Noy-Meir et al., 1989). In the semi-arid communities, those species, represented by P. sufruticosa and F. cretica, can be used as reliable indicators of degradation (Jauffret and Lavorel, 2003), and are favoured at the end of vegetation regression stages (Pettit et al., 1995; Liat et al., 1999) in most open sites (Landsberg et al., 1999) and reflect colonization and desertification processes. In contrast, sensitive species of the pristine matorral community, such as sclerophyllous small trees (Q. coccifera, O. europaea var. silvestrys) and glaucous dwarf-shrubs (Phlomis and Cistus spp.), decreased drastically with increasing grazing pressure and can be used as early indicators of grazing disturbance. Dwarf-palm (Ch. humilis), which was only affected by heavy grazing, and xeric thorny-shrubs, such as P. laevigata, which are well-adapted to moderate grazing, can be used in restoration programs. These species allows soil infiltration and nutrient retention around the plant crown, which promotes the facilitation of small-canopy shade-tolerant species in semi-arid ecosystems (Bertness and Callaway, 1994; Pugnaire and Haasse, 1996).

Acknowledgements This work was supported by the EU under its INCO-DC Program, contract number ERBIC18-CT98-0392: DRASME (Desertification risk Assessment in Silvopastoral Mediterranean Ecosystems) and by Spanish CICYT program, project number AMB1998-1017 (Evaluacioń de la presioń ganadera para la conservacioń de las estepas y matorrales Mediterrańeos). The support from both programs is gratefully acknowledged. We are grateful to Sandra Lavorel for comments on the manuscript.

Hairiness (HAIR) Spininess or thorniness (SPNY) Clonality (CLONA) Stem morphology (STMO) Leaf presence (LEPR) Leaf margins (REVO) Dormant bud position (DOBU)

Morphological Live cycle (LIFE) Plant coverage (PLCO) Leaf size (LESI) Leaf consistency (LECO) Leaf colour (LELO) + + +

0.25–2.25 cm2 ¼ 1/2.25–12.25 cm2 ¼ 0 Sclerophyllous ¼ 1/Mallacophyllous ¼ 0

Both sides with same colour ¼ 1/With different colour ¼ 0 Trichomes present ¼ 1/Absent ¼ 0 With spine or thorn ¼ 1/Absent ¼ 0

+

+ + +

Revolute ¼ 1/Non-revolute ¼ 0

Phanerophyte (41.5 cm high, trees, small trees, medium shrubs) ¼ 1/Non-phanerophyte (o1.5 cm high;—dwarf and half-shrubs) ¼ 0

+ +

+ +

+ +

+ +

Forbs

Clonal stems ¼ 1/Non-clonal stems ¼ 0 Rosette or palmiform stems ¼ 1/Nonpalmiform ¼ 0 Present ¼ 1/Absent (aphyllous) ¼ 0

+ +

+

Shrubs

Short lived ¼ 1/Perennial ¼ 0 o75–100 cm2 ¼ 1/475–100 cm2 ¼ 0

Description

+

+

+

Grasses

1,3

1

1

7 1

1 1,7

1,2

1,2 1,2

6 1,2

Source

316

Traits

List of traits used for the analysis within three groups: shrubs, forbs and grasses. 1 ¼ field observation and measurements, 2 ¼ Orshan (1982), 3 ¼ Raunkiaer (1934), 4 ¼ Faegry and van der Pijl (1979), 5 ¼ van der Pijl (1972), 6 ¼ McIntyre et al. (1999a), 7 ¼ Cornelissen et al. (2003).

Appendix

ARTICLE IN PRESS


o25–30 cm ¼ 1/425–30 cm ¼ 0

Inflorescence position (INPO) Main dispersal type (DITY)

Regeneration Reproduction type (RETY) Pollination type (POTY) Seed size (SESI) + + + + +

Sexual ¼ 1/Sexual and asexual ¼ 0

Anemophyllous ¼ 1/Enthomophyllous ¼ 0

Small ¼ 1(o2.25 mm2) ¼ 1/Medium or big (42.25 mm2) ¼ 0 Exposed ¼ 1/Protected ¼ 0

Wind ¼ 1/Others ¼ 0

Evergreen ¼ 1/Deciduous or semi-deciduous ¼ 0 +

o10–15 cm ¼ 1/415–30 cm ¼ 0

Phenological Deciduousness (DEDU)

Erect ¼ 1/Flat (prostrate) ¼ 0

Canopy structure (CAST) Lateral spread (LASP) Height (HEIG)

Shrubs

Description

Traits

Appendix (continued)

+

+

+

+

+

+

+

+

Forbs

+

+

+

+

+

+

Grasses

1,5,7

1,7

1

1,4

1

1,2

1

1

1

Source

ARTICLE IN PRESS

T. Navarro et al. / Journal of Arid Environments 64 (2006) 298–322 317



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