Dispersal traits and dispersal patterns in an oro-Mediterranean thorn cushion plant formation of the eastern High Atlas, Morocco

ARTICLE IN PRESS

Flora 204 (2009) 658–672 www.elsevier.de/flora

Dispersal traits and dispersal patterns in an oro-Mediterranean thorn cushion plant formation of the eastern High Atlas, Morocco Teresa Navarroa,, Jalal El Oualidib, Mohammed Sghir Talebc, Virginia Pascuala, Baltasar Cabezudoa a

Depto. de Biologı´a Vegetal, Universidad de Ma´laga. Apd. 59, 29080 Ma´laga, Spain De´part. de Botanique et Ecologie Ve´ge´tale, Institut Scientifique, Universite´ Mohammed V, B.P. 703, Agdal 10106, Morocco c Centre National de la Recherche Forestie`re, BP.763, Rabat 10005, Morocco b

Received 19 May 2008; accepted 20 August 2008

Abstract This study describes the dispersal traits and dispersal patterns of 51 perennial plant species belonging to 19 families in an oro-Mediterranean thorn cushion plant formation on the High Atlas, Morocco. Diaspore type, mass, number, antitelechoric mechanisms and dispersal time were studied with respect to growth forms, dispersal modes and spatial dispersal. Species spanned 105 range of diaspore mass, which coincided with those found in other high mountain regions. Diaspore mass was significantly higher in trees and shrubs than in semi-shrubs and perennial herbs. Barochorous and zoochorous species are more likely to have heavy diaspores, whereas anemochorous and ballistic species have a medium diaspore mass and semachorous and ombro-hydrochorous species have low diaspore mass. Diaspore number was significantly higher in trees and shrubs than in semi-shrubs and perennial herbs. The barochorous, ombro-hydrochorous and zoochorous species tended to produce higher diaspore numbers than species with other dispersal modes. Bradyspory was well-developed by trees and large shrubs dispersed by biotic vectors. Synaptospermy was represented by its long dispersal component. Myxospermy was significantly associated with semishrubs and perennial herbs with restricted spatial dispersal. It seems that ombro-hydrochory combined with myxospermy and a high number of light seeds is an efficient mechanism that ensures successful establishment of the most typical and endemic thorn cushion plant species, such as Alyssum, Vella and Ormenis. In our study area, the highest dispersal availability was synchronized with the dry summer season (July–August) and the beginning of the rainy months (September). The dispersal peak for the wind-dispersed species, which is the most effective primary dispersal mode, occurs during the dry season, while dispersal for the biotic-dispersed species takes place throughout the year. Published by Elsevier GmbH. Keywords: Antitelechoric mechanisms; Dispersal modes; Dispersal patterns; Diaspore traits; Growth forms; Mediterranean thorn cushion plant formation

Introduction Corresponding author.

E-mail address: [email protected] (T. Navarro). 0367-2530/$ - see front matter Published by Elsevier GmbH. doi:10.1016/j.flora.2008.08.005

Seed dispersal is a critical event in the regulation of floristic richness and species composition (Cain et al., 2000; Pa¨rtel et al., 1996). It is a key factor in

ARTICLE IN PRESS T. Navarro et al. / Flora 204 (2009) 658–672

conservation biology (Cooper and Walters, 2002; Haddad et al., 2003; Trakhtenbrot et al., 2005) and restoration management (Palmer et al., 1997). In high mountain ecosystems dispersal is an important driver in the spatial and temporal local distribution of species (Dirnbo¨ck and Dullingers, 2004), where the timing of dispersal is often the way by which germination is achieved at a favourable time (Frankie et al., 1974). There are few studies on the dispersal traits and dispersal patterns of perennial species in high mountain ecosystems, those which exist focus on herbaceous and grassland life forms (Ko¨rner, 2003; Thompson and Rabinowitz, 1989). However, knowledge of dispersal in perennial species is of relevance in the study of changes in oro-Mediterranean vegetation distribution, especially in the study of the migration process linked to climatic change (Cain et al., 2000; Clark, 1998; Parmesan and Yohe, 2003; Pauli et al., 2001). Angiosperms have developed different characteristics to ensure their successful dispersal (Tiffney, 1984). Seeds exhibit many different adaptations for dispersal (Snow, 1971), involving mass, shape and appendages (Willson and Thompson, 1982). Among dispersal traits, seed mass is a key functional trait (Kleyer, 1999; Weiher et al., 1999) in vegetation management (Dı´az and Cabido, 1997). This is related to many biological factors (Weiher et al., 1999), especially dispersal ability (Grime, 2001; Leishman et al., 1995; Thompson et al., 1998) and growth forms (Moles et al., 2005). Smaller and larger seeded species differ in their life-history strategies and the ability of a species to reach suitable regeneration sites does not depend only on how many seeds it produces, but also on how the seeds are dispersed (Coomes and Grubb, 2003). The oro-Mediterranean thorn cushion plant formations are unique biotic communities restricted to Mediterranean and Anatolian regions with a dry summer climate (Devillers et al., 2001). In the High Atlas National Park these formations play a vital role in traditional biodiversity mountain conservation (Taleb and Fennane, 2003, 2008). This study presents information about dispersal of 51 perennial species native to the High Atlas oroMediterranean thorn cushion plant formation, with information on taxonomic status. For each species, it includes growth form, diaspore type, diaspore mass, diaspore number per plant, dispersal mode, spatial dispersal ability, antitelechoric mechanisms and dispersal time. The antitelechoric mechanisms (Ehrman and Cocks, 1996; Ellner and Schmida, 1981; Van Rheede van Oudtshoorn and Van Rooyen, 1999; Van Rooyen et al., 1990) include bradyspory, myxospermy, basycarpy and synaptospermy, which protect diaspores from predation and other dangers and regulate the intraand inter-year timing of dispersal and germination (Gutterman, 1993, 1994, 2001). At the same time, plant

659

life traits and dispersal modes have been proposed to affect the dispersal phenology (Sarmiento and Monasterio, 1983; Snow, 1965). We assess whether dispersal patterns of an oro-Mediterranean thorn cushion plant formation follow the same tendency as the lowland Mediterranean scrublands. We also attempt to ascertain how antitelechoric mechanisms are developed in response to the particularity of this mountain habitat. This information is of utmost importance for the understanding and conservation of the few remaining areas and the application of management recommendations and restoration projects. We examined the dispersal traits in the High Atlas thorn cushion plant formation to answer the following questions: How are the diaspore mass, diaspore number and antitelechoric mechanisms related to growth forms, taxonomic groups, dispersal modes and spatial dispersal? What are the dispersal patterns in this vegetation type?

Materials and methods Study area The study was carried out in an oro-Mediterranean thorn cushion plant formation between 2167 and 2630 m a.s.l in a shallow north western facing slope in the eastern High Atlas National Park (321580 5700 N and 41560 6100 W), located 3 km north of Tirrhist (Canton of Tirrhist), Morocco. The climate is characterized by a dry summer season extending from June to the end of August and a rainy season extending from September to the end of February. The 24-year (1974–1998) mean maximum and minimum temperatures are 23 and 4 1C, respectively, and the annual precipitation is 401 mm (Taleb and Fennane, 2003). Three vegetation units were distinguished according to structure and composition (1) a Velletum mairei thorny cushion scrub (Que´zel, 1957) on the upper slope over rocky limestone substrate (AEFCS, 1996) with a canopy of 30–60% (2) a rock vegetation (Arenarietum dyris) (Que´zel, 1952) with an open canopy of 20% and (3) a Bupleuro spinosaeJuniperetum thuriferae montane forest (Que´zel, 1957) with a closed canopy of 40–70% on the less-inclined lower parts of the slope. The High Atlas vegetation like the most part of Mediterranean ecosystems has evolved in response to the joint pressure of a Mediterranean climate with a pronounced summer drought and human activities, particularly grazing for at least several millennia. It has experience in a long history of human impact, including grazing pressure and clearing activities. Grazing is light to moderate in the study site and mainly

Family and species

Apiaceae Bupleurum atlanticum Murb.

Growth Dispersal form mode

Spatial Diaspore dispersal type

Diaspore number, Seeds number Antitelechoric Dispersal Diaspore Diaspore mass appendages (weight), Mean and Mean and SD per diaspore mechanisms months SD

Twin fruit Vitta

3–4

A,D

Aug/Sept

Pher Pher Pher Pher

Anemochory Anemochory Anemochory Anemochory

Seed Seed Seed Seed

Pappus Pappus Pappus Pappus

758.97150 626.57175.52 283.57540.2 236.5773.88

1 1 1 1

– C C,D C

Jul/Aug Jul/Aug Jul/Aug Jul/Aug

Pher

OmbroRD hydrochory

Seed

0.8270.26

19,47879135.22

1

D

Jul/Aug

Brassicaceae a Matthiola scapifera Humbert Alyssum spinosum L.

Pher Ssh

RD RD

Vella mairei Humbert

Ssh

Biscutella frutescens Coss.

Pher

Anemochory Ombrohydrochory Ombrohydrochory Anemochory

– –

0.8070.22 3.0773.15

17887365.02 1 95,121761958.4 1–2(3)

B,C B,D

Jul Sept/Oct

Seed

–

1.3370.60

1

B,D

Sept/Oct

RD

Seed

–

0.0170

245.7574.82

1

–

Jun

Berberidaceae Berberis hispanica Boiss. & Reut. Sh

Zoochory

DDB

Berry

–

9.2872.87

1964.257696.92

2

A,D

Sept/Feb

Caprifoliaceae Lonicera pyrenaica L. Lonicera arborea Boiss. Viburnum lantana L.

Sh Sh Sh

Zoochory Zoochory Zoochory

DDB DDB DDB

Berry Berry Drupe

– – –

22.0676.41 45.1679.1 61.6776.76

6322.57832.95 6206.97809.36 28637689

6 1–2 1

A,D A,D D

Aug Aug Jul/Nov

Ssh Ssh

Anemochory RD Anemochory DDA

Seed Capsule

– Calyx hairs

100730.35 1 1166.47353.19 12–14

B A,B

Jul Jul

Cupressaceae Juniperus oxycedrus L.

Tr

Barochoryb DDB

Galbulus

–

462.79776.73

c

56,35673954.2

3

A,D

Juniperus communis L.

Tr

Barochoryb DDB

Galbulus

–

118.30730.15

c

50,20071809

3

A,D

Juniperus thurifera L.

Tr

Barochoryb DDB

Galbulus

–

237.35741.49

c

57,13573903

2–4

A,D

All seasons All seasons All seasons

Cistaceae Fumana thymifolia (L.)Webb Helianthemum croceum (Desf.) Pers.

0.4870.27

10477465.3

0.2770.7 19.4471.74 3.8870.69 7.15721.38

–

Seed Seed

RD

DDA DDA DDA DDA

2.6270.67 2.5672.55

32877913.13

ARTICLE IN PRESS

Anemochory DDA

T. Navarro et al. / Flora 204 (2009) 658–672

Ssh

Asteraceae Atractylis serratuloides Sieb. a Carduncellus atractyloides Batt. a Catananche caespitosa Desf. a Scorzonera pygmaea Sibth. & Sm. b Ormenis scariosa (Ball) Litard & Maire

660

Table 1. Scientific name (including author), family, growth form, diaspore traits, dispersal patterns, antitelechoric mechanisms and dispersal time for each of the 51 studied species in the oro-Mediterranean thorn cushion plant formation on the High Atlas, Morocco.

Ephedraceae Ephedra nebrodensis Tineo ex Guss.

Pseudocarp

Ssh

Ballistic

RD

Ssh

Ballistic

RD

Seed with – elaiosome Seed with – elaiosome

Fabaceae Astragalus granatensis Lam. b Astragalus ibrahimianus Maire Astragalus incanus L. Coronilla minima L. Cytisus balansae (Boiss.) Ball

Ssh Ssh Ssh Ssh Sh

Anemochory Anemochory Anemochory Anemochory Ballistic

DDA DDA DDA DDA RD

Erinacea anthyllis Link Genista scorpius (L.) DC Medicago suffruticosa DC Ononis cristata Mill. b Ononis atlantica Ball

Ssh Sh Pher Ssh Ssh

Ballistic Barochory Barochory Ballistic Anemochory

RD DDA DDA RD DDA

Globulariaceae b Globularia nainii Batt.

Ssh

Grossulariaceae Ribes uva-crispa L.

Euphorbiaceae b Euphorbia megalatlantica Ball a

Euphorbia nicaeensis All.

Lamiaceae b Marrubium ayardii Maire b Marrubium multibracteatum Humbert & Maire Salvia phlomoides Asso a Teucrium chamaedrys L. Teucrium aureum subsp. flavovirens (Batt.) Puech Thymus pallidus Batt. Oleaceae Fraxinus dimorpha Coss. & Durieu

15.0471.49

c

3.9770.59 4.5174.30

38,6337786.21

1–2

A,D

Jun/Aug

7407338.79

2–3

–

Aug

2–3

–

Aug

2847123.48 2 10107366 4 90.1717.64 6–10 47714.51 2–3(5) 963.97490.9 1

A A A A

Jul Jul May Jul Aug

1 2–4 3–5 1 3–4

– A A – A

Aug Jul Jul Aug Jun

1

D

Jul/Aug

235.79763.73

Pod Pod Pod Pod Seed with elaiosome Seed Pod Pod Seed Pod

– – Calyx

10.8571.66 40.49739 36.2975.8 1.4270.49 7.3271.34

OmbroDDA hydrochory

Achene

Wing

1.1870.4

Sh

Zoochory

DDB

Berry

–

40.23713.74

952.90713.74

6

A,D

May/Aug

Ssh Ssh

Semachory Semachory

RD RD

Nutlet Nutlet

– –

0.3770.09 0.2070.08

867.157212.6 625.17118.93

1 1

D D

Jul/Sept Jul/Sept

Ssh Ssh Ssh

Semachory RD Semachory RD Anemochory DDA

– – Hairs

4.9972.42 0.9770.42 3.3370.75

460.57199.9 103.7771.73 237.6799.6

1 1 1–2

– – A,D

Jul Jul Jul/Sept

Ssh

Anemochory DDA

Nutlet Nutlet Calyx hairs Calyx hairs

Hook

3.7570.33

8487465.68

1–4

A,D

Jul/Sept

Tr

Anemochory DDA

Samara

Wing

97.1674.45

52,22873289.5

1

–

Sept

Seed

–

480.67224.6

1

B,D

Jul/Aug

Pher

RD

Calyx hairs 29.5477.39 Calyx hairs 17.8074.29 Calyx hairs 53.61712.11 Calyx 9.1972.13 – 6.0171.45 –

1.5971.6

1044.77540.2 8397277.24 128.757168 1772.34 1471.97275.55 322072790.46

c

661

Plantaginaceae a Plantago coronopus L.

Bracts

ARTICLE IN PRESS

Barochoryb DDB

T. Navarro et al. / Flora 204 (2009) 658–672

Sh

Family and species

a

Plantago mauritanica Boiss. & Reuter

662

Table 1. (continued ) Growth Dispersal form mode

Ssh

Spatial Diaspore dispersal type

Ombrohydrochory OmbroRD hydrochory Zoochory

DDB

Prunus prostrata Labill.

Sh

Zoochory

DDB

Rosa canina L.

Sh

Zoochory

DDB

Scrophulariaceae Digitalis lutea L. Linaria tristis (L.) Mill.

Pher Pher

Semachory Semachory

RD DDA

Tr Sh

Sh

Rhamnaceae Rhamnus alpina L. b Rhamnus lycioides subsp. atlantica (Murb.) Jahand. & Maire Thymelaeaceae Daphne laureola L.

Aggregate – follicle Aggregate – follicle Aggregate – follicle

1.5870.6

206.37114.1

329.46726.56

1937.587749.34

115.84717.48

29.25710.62

B,D

Jul/Aug

2–3

A,D

Sept/Feb

D

Sept/Feb

A,D

Sept/Feb

– –

Aug Apr/May

A,D A,D

Jul/Sept Jul/Sept

D

Jul/Sept

1

139.257125.7

2061.357832.65 25–30

1.4271.4 0.0170

8387564.41 1 1132.77168 30–40

Seed Seed

– Wing

Barochoryd DDB Barochoryd DDB

Drupe Drupe

– –

15.3172.65 18.8674.6

Zoochory

Berry

–

15.4772.7

DDB

1

c

48,88873032.8 29,491.873854.54

19277763.17

2–4 2–4

1

Growth forms: Pher, perennial herbs; Ssh, semi-shrubs; Sh, shrubs; Tr, trees. Spatial dispersal: RD, restricted spatial dispersal; DDA, developed spatial dispersal by abiotic vectors; DDB, developed spatial dispersal by biotic vectors. Antitelechoric mechanisms: A, synaptospermy; B, myxospermy; C, basycarpy; D, bradyspory. a Vegetatively spread species. b Endemic species from the High Atlas National Park, Morocco. c Mature trees and large shrubs. d These diaspores often fall close to the parent plant, but may also be secondarily transported by vertebrates.

ARTICLE IN PRESS

Tr

–

T. Navarro et al. / Flora 204 (2009) 658–672

Rosaceae Crataegus laciniata Ucria

Seed

Diaspore Diaspore mass Diaspore number, Seeds number Antitelechoric Dispersal appendages (weight), Mean and Mean and SD per diaspore mechanisms months SD

ARTICLE IN PRESS T. Navarro et al. / Flora 204 (2009) 658–672

occurs in spring. In the study site the ecosystem management is regulated by the Moroccan government.

Selection of species Field sampling and phenological observations were carried out monthly between December 2005 and November 2007. The number of species in this study represents a cross-section of vegetation and importance was given to incorporate all common and rare perennial species that characterize the vegetation (Taleb and Fennane, 2003, 2008). Species dominance had been previously assessed with the relative importance values (Taleb and Fennane, 2003, 2008) in which the abundance of the species has been estimated according to the Braun Blanquet scale (Braun Blanquet, 1952). We discarded all the species that were present in less than 10% of all the releve´s available. The selected perennial dominant species probably represent ca. 80% of the total cover in the studied site. Voucher specimens of the studied species were kept in the RAB and MGC Herbaria. Botanical nomenclature follows Fennane et al. (1999/2007) and Castroviejo et al. (1986–2007). The family and class affiliation of each species were added using the APG II (Angiosperm Phylogenetic Group, 2003). Seven easily measured dispersal traits and four antitelechoric mechanisms (Table A1) were analysed. Among dispersal traits, the dispersal mode and diaspore mass (weight) constitute the main regenerative traits according to Cornelissen et al. (2003). Based on growth form, species were classified as (i) trees and shrubs: woody plants taller than 0.8 m with main canopy deployed relatively close to the soil surface on one or more relatively short trunk/s, (ii) semi-shrubs: woody plants up to 0.8 m tall (chamaephytes) and (iii) perennial herbs (Cornelissen et al., 2003). All semi-shrubs were chamaephytic species. The term diaspore was used to name the dispersal unit (Weiher et al., 1999). Whenever a diaspore lent itself to more than one type of dispersal mode, the mechanism judged to be predominant was assigned. The achenes of Asteraceae were measured with the pappus. Diaspores were collected when ripe but before they started to fall off the plant. For each individual, 20 diaspores (100 for small seeded species) were air-dried and measured (Cornelissen et al., 2003). We determined the number of diaspores per plant in 20 adult plants of a given species growing in a typical habitat and exposed to full sunlight. For mature trees and large shrubs, the number of diaspores was determined following Knevel et al. (2005). We considered that species with developed spatial dispersal are those whose diaspores are equipped with structures that facilitate spatial dispersal, such as flyer structures (pappi, barbs, wings) (dispersed by abiotic vectors) or

663

fleshy fruits (dispersed by biotic vectors) according to Ellner and Schmida (1981), Venable and Levin (1985), Cain et al. (2000) and Higgins et al. (2003), and we considered species with restricted spatial dispersal those whose diaspores lack such dispersal-enhancing characters, following Willson (1993). The antitelechoric mechanisms (Van Rheede van Oudtshoorn and Van Rooyen, 1999) include bradyspory, basicarpy (Van Rooyen et al., 1990; Zohary, 1962), synaptospermy (Ellner and Schmida, 1981; Van Rooyen et al., 1990; Zohary, 1937, 1962) and myxospermy (Van Rooyen et al., 1990; Zohary, 1937). Bradyspory (dispersal in time) was indicated for those species with delayed diaspore release, which are all or partially retained and protected by the lignified floral structures and by dry and fleshy fruits. The frequency of species belonging to different categories in dispersal modes and spatial dispersal was calculated every month. Species, family, growth form, dispersal traits and dispersal time are presented in Table 1.

Statistical analyses One-way analysis of variance (ANOVA) was used to test the significance of differences (Po0.01) of diaspore mass (weight), and diaspore number among dispersal modes and spatial dispersal. To examine differences in diaspore mass and number among growth forms and taxonomic class rank, we used the Kruskal–Wallis test (K–W) after categorization of the variables. The diaspore mass was grouped into nine categories:o0.3, 0.31–1, 1.1–3, 3.1–9, 9.1–30, 31–90, 91–300, 301–900, 4901 mg, while the diaspore number per plant was grouped into six categories: 0–250, 251–500, 501–1000,

Fig. 1. Frequency distribution of dispersal modes of 51 perennial species in an oro-Mediterranean thorn cushion plant formation of High Atlas National Park, Morocco.

ARTICLE IN PRESS 664

T. Navarro et al. / Flora 204 (2009) 658–672

1001–2500, 2501–5000, 45001 following Bekker and Kwak (2005). The association between nominal traits was determined with the Pearson w2 test-statistic. Correlations between quantitative traits were examined using Pearson correlation coefficient. Diaspore mass and diaspore number were log-transformed prior to statistical analysis. One-way analysis of variance ANOVA was applied after verifying the homogeneity of variance by Levene’s test. All statistical analyses were performed with SPSS 14. The original matrices are available on request.

Fig. 2. Frequency distribution of diaspore types of 51 perennial species in an oro-Mediterranean thorn cushion plant formation of High Atlas National Park, Morocco.

Results Dominant growth forms were the semi-shrubs (22 species, 43.1%), followed by shrubs (12 species, 23.5%), perennial herbs (11 species, 21.6%), and lastly trees (6 species, 11.8%). Anemochorous (17 species, 33.3%) were dominant followed by zoochorous (9 species, 17.6%), barochorous (8 species, 15.6%), ombro-hydrochorous (6 species, 11.7%) and semachorous (6 species, 11.7%) and lastly ballistics (5 species, 9.8%) (Fig. 1). Eighteen species (35.3%) had restricted spatial dispersal, and 33 species (64.7%) were species with a developed spatial dispersal ability. Among them, 15 species (29.4%) were dispersed by biotic vectors (mainly vertebrate-dispersal) and 16 species (35.3%) by abiotic vectors (wind). The seeds were the dominant diaspore type (19 species, 37.3%), followed by pods (7 species, 13.7%) and berries (5 species, 9.8%) (Fig. 2). Within the pod category, 42.8% of the pods were provided with multiple appendages (calyx, hairs and awns) belonging to species of the genera Astragalus, Coronilla and Ononis (Fig. 3A). Another diaspore provided with appendages (calyx) was the capsule of Helianthemum croceum (Fig. 3B). Within the seed category, 21% were seeds with pappus, belonging to species of the genera Atractylis, Scorzonera, Catananche and Carduncellus (Fig. 3C). A total of 15.7% were seeds with elaiosomes produced by species of Euphorbia and Cytisus (Fig. 3D) (Table A1). In our study area, 52.9% (27 species) retained their diaspores on the mother plant after maturation. A total of 13.7%

Fig. 3. Diaspore types: (A) pod of Astragalus granatensis, (B) capsule of Helianthemum croceum, (C) seed of Carduncellus atractyloides and (D) seed of Euphorbia megalatlantica.

ARTICLE IN PRESS T. Navarro et al. / Flora 204 (2009) 658–672

(7 species) were myxospermics (100% of species belonging to Cistaceae and Plantaginaceae) and 9.8% (4 species) were basycarpics (Table 1). A total of 15.6% (8 species) were vegetative spreading species (62.5% of them with restricted spatial dispersal) (Table 1).

Diaspore mass Diaspore mass ranged from 0.01 mg in Linaria tristis (Scrophulariaceae) and Biscutella frutescens (Brassicaceae) to 462.79 mg in Juniperus oxycedrus (Cupressaceae) (Table 1), with a mean of 39.45 mg (Table 2). Cupressaceae, Rosaceae and Oleaceae were the families with the heaviest diaspores (Table 2). The frequency of diaspore mass classes on a logarithmic scale produced an approximately normal distribution (Fig. 4). Within the High Atlas oro-Mediterranean thorn cushion plant

665

formations, perennial species spanned 105 range of diaspore mass from 106 to 101 g. Diaspore mass was significantly higher in Coniferopsida than in Angiosperms and higher in Eudicots and Eurosids I than in Eurosids II and Euasterids (K–W: H ¼ 17.03, Po0.01, Table 2, Fig. 5A). Diaspore mass was significantly higher in trees and shrubs than in semishrubs and perennial herbs (K–W: H ¼ 23.8, Po0.01, Fig. 5B). Semi-shrubs were likely to have medium diaspore mass, while perennial herbs were likely to have medium or low diaspore mass. The ANOVA revealed significant differences in diaspore mass among dispersal modes (F ¼ 7.77, df ¼ 5, Po0.01) and spatial dispersal (F ¼ 20.03, df ¼ 2, Po0.01). Barochorous and zoochorous species are more likely to have heavy diaspores, whereas the anemochorous and ballistic species have medium diaspore mass and semachorous and ombro-hydrochorous species

Table 2. Descriptive statistics for diaspore mass and diaspore number per plant in families for 51 species studied in the oroMediterranean thorn cushion plant formation of High Atlas National Park, Morocco. Families

N

Diaspore Mass (mg)

Diaspore number

Mean

SD

Minimum

Maximum

Mean

Spermatopsida Coniferopsida Ephedraceae Cupressaceae

1 3

15.04 272.81

– 174.96

15.04 118.30

15.04 462.79

38,633 54,563.66

Angiosperms Eudicots Berberidaceae Grossulariaceae

1 1

9.28 40.23

– –

9.28 40.23

9.28 40.23

1964.25 589.39

Eurosids I Fabaceae Rosaceae Euphorbiaceae Rhamnaceae

10 3 2 2

21.25 194.85 4.24 17.08

17.62 117.16 0.381 2.51

1.42 115.84 3.97 15.31

53,61 329.46 4.51 18.86

Eurosids II Brassicaceae Cistaceae Thymelaeaceae

4 2 1

1.12 2.59 15.47

1.30 0.04 –

0.01 2.56 15.47

Euasterids I Plantaginaceae Globulariaceae Oleaceae Lamiaceae Scrophulariaceae

2 1 1 6 3

1.58 1.18 97.16 2.27 21.03

0.00 – – 1.99 35.20

Euasterids II Apiaceae Asteraceae Caprifoliaceae

1 5 2

0.48 6.31 26.97 39.4527

Total

51

SD

– 3799.06

Minimum

Maximum

38,633 50,200

38,633 57,135

– –

1964.25 952.90

1964.25 952.90

589.39 1406.33 487.89 39,154.50

531.41 1219.13 356.53 9733.50

17 39 235.79 29421

1471.90 2380 740 48,888

3.07 2.62 15.47

25,110.43 633.00 1927.00

46,690.22 753.77 –

245.75 100 1927

1.58 1.18 97.16 0.20 0.01

1,59 1.18 97.16 4.99 61.67

823.50 1381.08 52,228 523.67 1680.13

484.93 – – 315.15 1025.33

480.60 3220 52,228 103 1044.70

– 7.83 25.71

0.48 0.27 8.79

0.48 19.44 45.16

1048 4276.68 6264

– 8500.89 82.04

1048 236.50 6206

1048 19,478 6322

86.310

0.01

462.79

9779.83

20,558.03

17

95,121

Taxonomic groups affiliation of families follows the APG II (Angiosperm Phylogenetic Group) (2003).

95,121 1166 1927 1166.40 3220 52,228 867.15 2863

ARTICLE IN PRESS 666

T. Navarro et al. / Flora 204 (2009) 658–672

have low diaspore mass (Fig. 5C). In our study area there is a clear tendency for species with developed spatial dispersal to have heavier diaspores than those with restricted spatial dispersal (Fig. 5D).

Diaspore number

Fig. 4. Diaspore mass distribution of 51 perennial species in an oro-Mediterranean thorn cushion plant formation of High Atlas National Park, Morocco.

Diaspore number ranged from 17 in Ononis cristata (Fabaceae) to 95121 in Alyssum spinosum (Brassicaceae) (Table 1), with a mean of 9779.9 (Table 2). Cupressaceae, Oleaceae, Eephedraceae, Rhamnaceae and Brassicaceae were the families with the highest number of diaspores (Table 2). Diaspore number was significantly higher in trees and shrubs than in semi-shrubs and perennial herbs (K–W: H ¼ 17.89, Po0.01, Fig. 6A). A total of 83.3% of the trees produce a diaspore number over 5000, whereas

Fig. 5. Box plots showing median, quartiles, outliers (O) and extremes (*) of diaspore mass (log) of 51 perennial species in an oroMediterranean thorn cushion plant formation of High Atlas National Park, Morocco. (A) diaspore mass grouped by the APG II taxonomic groups affiliation, (B) grouped by growth forms, (C) grouped by dispersal modes and (D) grouped by spatial dispersal.

ARTICLE IN PRESS T. Navarro et al. / Flora 204 (2009) 658–672

667

72% of perennial herbs produce a diaspore number under 1000. The ANOVA revealed significant differences in diaspore number among dispersal modes (F ¼ 7.65, df ¼ 5, Po0.01) and spatial dispersal (F ¼ 5.38, df ¼ 2, Po0.01). Our results show how, among dispersal modes, the barochorous, ombro-hydrochorous and zoochorous species tend to produce a higher diaspore number than the species with another dispersal mode (Fig. 6B). A total of 66.6% of barochorous species produce a diaspore number over 5000, whereas 83.3% of semachorous species produce a diaspore number under 1000. Species with developed spatial dispersal by biotic vectors tend to produce a higher diaspore number (57.14% of them produce over 5000 diaspores) than those dispersed by abiotic vectors (except for Fraxinus dimorpha), or those with restricted spatial dispersal (Fig. 6C). A total of 44.4% of species with restricted spatial dispersal produce a diaspore number under 500 (except for A. spinosum, Ormenis scariosa and O. cristata) (Fig. 6C).

Antitelechoric mechanisms Bradyspory was significantly associated with growth forms (w2 ¼ 10.86, df ¼ 3, Po0.01) and spatial dispersal (w2 ¼ 12.9, df ¼ 2, Po0.01). The number of bradysporic species was higher within trees (5 species, 83.3%) and shrubs (10 species, 83.3%) than within semi-shrubs (9 species, 40.9%) or perennial herbs (3 species, 27.27%) (Fig. 7). All species with developed spatial dispersal by biotic vectors were bradysporic, whereas only 5 species (31.2%) with developed spatial dispersal by abiotic vectors and 6 species (33.3%) with restricted spatial dispersal were bradysporic (Fig. 8). There was a relationship between synaptospermy and spatial dispersal (w2 ¼ 12.94, df ¼ 2, Po0.01). Plants with synaptospermy were more represented in the spatial dispersal by biotic (12 species, 80%) and by abiotic (11 species, 68.7%) vector categories. Species with restricted spatial dispersal lack synaptospermy (Fig. 9). Myxospermy was also related with spatial dispersal (w2 ¼ 9.30, df ¼ 2, Po0.01). Species with myxospermy were more represented in restricted spatial dispersal (6 species, 33.3%) and less represented in the developed spatial dispersal by abiotic vectors (1 species, 6.6%) categories. Species with developed spatial dispersal by biotic vectors lack myxospermy (Fig. 10).

Dispersal patterns Fig. 6. Box plots showing median, quartiles, outliers (O) and extremes (*) of diaspore number (log) of 51 perennial species in an oro-Mediterranean thorn cushion plant formation of High Atlas National Park, Morocco. (A) diaspore number grouped by growth forms, (B) grouped by dispersal modes and (C) grouped by spatial dispersal.

Major dispersal occurred during the dry summer season (July–August) (40 species, 78.43%) and at the beginning of the rainy season (September) (19 species, 37.25%). The lowest number of dispersal species was

ARTICLE IN PRESS 668

T. Navarro et al. / Flora 204 (2009) 658–672

Fig. 7. Bradyspory and growth form of 51 perennial species in an oro-Mediterranean thorn cushion plant formation of High Atlas National Park, Morocco.

Fig. 8. Bradyspory and spatial dispersal of 51 perennial species in an oro-Mediterranean thorn cushion plant formation of High Atlas National Park, Morocco.

found in March (3 species) (Fig. 11A). The highest dispersal for the anemochorous (13 species) and the semachorous species (4 species) occurs in July (Fig. 11A). Both species groups showed a similar tendency of variation in monthly number of dispersal (r ¼ 0.949, Po0.01). Zoochorous species increase dispersal from the late dry season until the beginning of the rainy months (end August–September), when a dispersal peak occurs (6 species), whereas barochorous species disperse all year with a peak in July (7 species). Spatial dispersal

Fig. 9. Synaptospermy and spatial dispersal of 51 perennial species in an oro-Mediterranean thorn cushion plant formation of High Atlas National Park, Morocco.

Fig. 10. Myxospermy and spatial dispersal of 51 perennial species in an oro-Mediterranean thorn cushion plant formation of High Atlas National Park, Morocco.

species (by biotic vectors) are spread throughout the year with a peak at the beginning of the rainy months (11 species, 55%), whereas abiotic dispersal takes place from April–September, reaching a dispersal peak in July (13 species, 42.8%). The highest dispersal for restricted spatial dispersal species was found in August (11 species, 61.1%) (Fig. 11B) coinciding with the peak of the ballistic species (5 species) (Fig. 11A). Ombro-hydrochorous

ARTICLE IN PRESS T. Navarro et al. / Flora 204 (2009) 658–672

669

Fig. 11. Number of species observed in six dispersal modes (zoochory, semachory, barochory, ombro-hydrochory, anemochory, ballistic dispersal) (A), and in three spatial dispersal categories (restricted spatial dispersal, developed spatial dispersal by biotic vectors and by abiotic vectors). (B) occurred in each month and monthly rainfall in the oro-Mediterranean thorn cushion plant formation of High Atlas National Park, Morocco. Average monthly rainfall (1974–1998).

species synchronize their dispersal with the rainy season (Fig. 11A).

Discussion There are few, if any, reports on diaspore characteristics and dispersal patterns in the oro-Mediterranean thorn cushion plant formations, which is particularly important for comparative ecological studies and for developing scientific conservation initiatives in mountain ecosystems (Finckh, 2006; Finckh and Staudinger, 2002). Our results show how the High Atlas oroMediterranean thorn cushion plant formations follow the general trends established for lowland Mediterranean scrublands, where wind-dispersal is the most effective primary dispersal mode (Guitia´n and Sa´nchez, 1992; Hensen, 1999; Jurado et al., 2001; Van Rooyen et al., 1990). Wind-dispersal is well represented by the endemic and most typical thorn cushion plant formation species. This is the case of Astragalus spp. which produces indehiscent pods provided with multiple appendages acting like balloons rolling over the ground.

This behaviour is typical of Fabaceae inhabiting deserts (Gutterman, 1993). It seems to be a successful dispersal also in the High Atlas thorn cushion plant formation. Another example is represented by Teucrium aureum and Thymus pallidus, which are dispersed by the papery persistent calyx acting as a closed balloon. This diaspore type has been described as typical of open dry vegetation (Dansereau and Lems, 1957; El Oualidi et al., 1996; Navarro et al., 1993, 2006). Compared with other floras (Baker, 1972; Jurado et al., 1991, 2001; Leishman et al., 2000; Zhang et al., 2004), the diaspore mass range for perennial species from the High Atlas oro-Mediterranean thorn cushion plant formation coincided with the range found in the subalpine meadow of the Tibetan plateau (Zhang et al., 2004) but with one order more of magnitude. Our results agree with the previous ones suggesting that the selection would favour smaller seeds in low productivity mountain environments (Zhang et al., 2004). In the case of the oro-Mediterranean thorn cushion plant formation, the plants with smaller seeds correspond with the ombro-hydrochorous and semachorous species. In addition, all dispersal modes are feasible in the diaspore mass ranging between 102 and 103 g, which suggests

ARTICLE IN PRESS 670

T. Navarro et al. / Flora 204 (2009) 658–672

that it is the most performing diaspore mass range in our study area. The Angiosperm families represented in the High Atlas thorn cushion plant formation produce smaller seeds than Coniferopsida, in agreement with statements by Moles et al. (2005), and the Rosid species tend to have larger diaspores than the Asterids. In the High Atlas oro-Mediterranean thorn cushion plant formation, the species with heavy diaspores were vertebrate-dispersed shrubs and trees from Cupressaceae, Rosaceae, Rhamnaceae and Berberidaceae families. This is in accordance with findings of Jurado et al. (1991, 2001), Leishman and Westoby (1994), Hughes et al. (1994), Metcalfe and Grubb (1995), Westoby et al. (1996). Similar as in the previous studied, also in the High Atlas thorn cushion formation, a larger diaspore mass is typically associated with larger growth forms of the plants (cf. Dı´az and Cabido, 1997; Jurado et al., 1991). Species with developed spatial dispersal were dominant (64.7%) in the High Atlas thorn cushion plant formation. However, the percentage of species with restricted spatial dispersal is relatively high (35.3%), which mainly corresponds with the ombro-hydrochorous and ballistic species. This demonstrates how restricted spatial dispersal might be selected under certain climatic conditions ensuring plant survival and establishment (Lavorel et al., 1994), and how restricted spatial dispersal appears to be a more common phenomenon in alpine vegetation (Ko¨rner, 2003). It seems that ombro-hydrochory combined with myxospermy and with a high number of light seeds is an efficient mechanism that ensures successful establishment for the most typical thorn cushion plants, such as Alyssum, Vella, Ormenis and Plantago species. On the other hand, the Fabacean Ononis, Cytisus and Erinacea species with ballistic dispersal have an important functional role in the High Atlas thorn cushion plant formation as they reinforce the plant spatial aggregation and favour plant survival in situ (Puigdefabregas and Pugnaire, 1999). Bradyspory, synaptospermy and myxospermy were the antitelechoric mechanisms best represented in our study area. Bradyspory was common for trees and large shrubs dispersed by biotic vectors. This mechanism is important for dispersal in time and for the colonization of establishment sites. Synaptospermy was represented by plants with long dispersal period (Ellner and Schmida, 1981). This mechanism is advantageous in the High Atlas thorn cushion plant formation because it protects the diaspores against mechanical damage and spreads germination over time until there are favourable conditions (Ellner and Schmida, 1981; Van Rheede van Oudtshoorn and Van Rooyen, 1999). The percentage of species developing myxospermy is similar to that found in other arid regions (11% in Saharan North Africa – Murbeck, 1919 – and 11% in Namaqualand, South

Africa – Van Rooyen et al., 1990). This demonstrates how myxospermy is also an efficient mechanism in high mountain thorn cushion plant formations protecting diaspores from predation and favours entrapment (Henko et al., 1998). Basycarpy was restricted to perennial herbs of small stature belonging to Asteraceae and Brassicaceae families, which agrees with information given by Van Rheede van Oudtshoorn and Van Rooyen (1999). In our study area, the dispersal peak for the species dispersed by abiotic vectors (wind) occurs in synchronization with the dry season, as it is the case also in other regions with climatic restrictions (Navarro et al., 1993; Van Rooyen et al., 1990). In the High Atlas thorn cushion plant formation, dryness favoured the more efficient dispersion of the pod, capsule, calyx and other balloon diaspores due to the stronger winds at the end of the dry months (Augspurger and Franson, 1987), while dispersal for the biotic-dispersed species occurred throughout the year. Ombro-hydrochrous plants synchronized their dispersal at the beginning of the rainy months (end August–September). This represents a suitable plant survival strategy in response to the seasonal changes. Dispersal of these species depends on the first rains, and this provides germination in the most favourable time and allows the permanent occupation of a favourable site (Gutterman, 1994; Sobral Griz and Machado, 2001). For restoration projects, seed-collection effort should be carried out during the months when the highest number of species is in dispersal phase (July–August). For biodiversity conservation, it is recommended that the use of vegetation as a natural resource (e.g. clearing human activities) should be restricted during the dry period and the beginning of the rainy season (July– September). Finally, perennial species with a spatial restricted dispersal and with antitelechoric mechanisms (e.g. A. spinosum, Vella mairei, Erinacea anthyllis) must be carefully observed in conservation planning if we wish to protect biological diversity.

Acknowledgement We gratefully acknowledge the support of the Spanish AECI (PCI Morocco, A/6534/07) ‘‘Regeneration strategies of perennial plants species in natural ecosystems of Morocco’’.

References AEFCS, 1996. Plan Directeur des aires Prote´ge´es du Maroc. Vol. 1–5. Adm. Ge´n. Eaux et Foreˆts et Cons. Sols/ BCEOM-SECA.

ARTICLE IN PRESS T. Navarro et al. / Flora 204 (2009) 658–672

APG II. (Angiosperm Phylogenetic Group), 2003. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants. APG II. Bot. J. Linn. Soc. 141, 339–436. Augspurger, C.K., Franson, S.E., 1987. Wind dispersal of artificial fruits varying in mass, area and morphology. Ecology 68, 27–42. Baker, H.G., 1972. Seed weight in relation to environmental conditions in California. Ecology 53, 997–1010. Braun Blanquet, J., 1952. Phytosociologie applique´. I. Comm. S.I.G.M.A. 116, 156–161. Bekker, M.R., Kwak, M.M., 2005. Life history traits as predictors of plant rarity, with particular reference to hemiparasitic Orobanchaceae. Folia Geobot. Phytotaxon. 40, 231–242. Cain, M.L., Milligan, B.G., Strand, A.E., 2000. Long-distance seed dispersal in plant population. Am. J. Bot. 87, 1217–1227. Castroviejo, S., et al. (Eds.), 1986/2007. Flora Ibe´rica. vols. I–VX. Real Jardı´n Bota´nico. CSIC, Madrid. Clark, J.S., 1998. Why trees migrate so fast: confronting theory with dispersal biology and the paleorecord. Am. Nat. 152, 204–224. Coomes, D.A., Grubb, P.J., 2003. Colonization, tolerance, competition and seed-size variation within functional groups. Trends Ecol. Evol. 18, 283–291. Cooper, C.B., Walters, J.R., 2002. Experimental evidence of disrupted dispersal causing decline of an Australian passerine in fragmented habitat. Conserv. Biol. 16, 471–478. Cornelissen, J.H.C., Lavorel, S., Garnier, E., Dı´az, S., Buchmann, N., Gurvich, D.E., 2003. A handbook of protocols for standardized and easy measurement of plant functional traits worldwide. Aust. J. Bot. 51, 335–380. Dansereau, P., Lems, K., 1957. The Grading of Dispersal Types in Plant Communities and their Ecological Significance. Contribution H. L’Institut Botanique de L’Universite de Montreal, Montreal. Devillers, P., Devillers-Terschuren, J., Van der Linden, C., 2001. Palaearctic Habitats. PHYSIS Data Base, 1996. Dı´az, S., Cabido, M., 1997. Plant functional types and ecosystem function in relation to global change. J. Veg. Sci. 8, 463–474. Dirnbo¨ck, T., Dullinger, S., 2004. Habitat distribution models, spatial autocorrelation, functional traits and dispersal capacity of alpine plant species. J. Veg. Sci. 15, 77–84. Ehrman, T., Cocks, P.S., 1996. Reproductive patterns in annual legume species on an aridity gradient. Vegetatio 122, 47–59. Ellner, S., Schmida, A., 1981. Why are adaptations for longrange seed dispersal rate in desert plants? Oecologı´a 51, 133–144. El Oualidi, J., Martin, A., Puech, S., 1996. Le polymorphisme du calice chez Teucrium dunense (Labiatae): son maintien sur les dunes du littoral. Acta Bot. Gallica 143 (1), 55–63. Fennane, M., Ibn Tattou, M., Mathez, J., Ouyahya, A., El Oualidi, J., (Eds.), 1999/2007. Flore Pratique du Maroc. Vols. 1–2. Trav. Inst. Sci. Ser. Bot. no 38. Rabat. Finckh, M., 2006. Klima- und Landnutzungsgetriebene Dynamik von Vegetationsmustern in Su¨dmarokko. Ber. Reinh. Tu¨xen-Ges. 18, 83–99.

671

Finckh, M., Staudinger, M., 2002. Mikro-und makroskalige Ansa¨tze zu einer Vegetationsgliederung des Draˆa-Einzugsgebietes (Su¨dmarokko). Ber. Reinh. Tu¨xen-Ges. 14, 81–92 Hannover. Frankie, G.W., Baker, H.G., Opler, P.A., 1974. Comparative phenological studies of trees in tropical wet and dry forests in the lowlands of Costa Rica. J. Ecol. 62, 881–919. Grime, J.P., 2001. Plant Strategies, Vegetation Processes, and Ecosystem Properties. Wiley, Chichester. Guitia´n, J., Sa´nchez, J.M., 1992. Seed dispersal spectra of plant communities in the Iberian Peninsula. Vegetatio 98, 157–164. Gutterman, Y., 1993. Seed Germination in Desert Plants. Adaptation of Desert Organisms. Springer, Berlin. Gutterman, Y., 1994. Strategies of seed dispersal and germination in plants inhabiting desert. Bot. Rev. 60, 371–425. Gutterman, Y., 2001. Regeneration of Plants in Arid Ecosystems Resulting from Patch Disturbance. Geobotany 27, Kluwer, Dordrecht. Haddad, N.M., Bowne, D.R., Cunningham, A., Danielson, B.J., Levey, D.J., Sargent, S., Spira, T., 2003. Corridor use by diverse taxa. Ecology 84, 609–615. Henko, V., Galena, S., Van der Maarel, E., 1998. Population strategies in severe environments: alpine plants in the northwestern Caucasus. J. Veg. Sci. 9, 27–40. Hensen, I., 1999. Life strategies of semi-desert plants: mechanisms of dispersal and reproduction in the thermomediterranean shrubland community Anabasio-euzomodendretum bourgaeani. An. Jard. Bot. Madrid 57 (1), 63–79. Higgins, S.I., Nathan, R., Cain, M.L., 2003. Are long-distance dispersal events in plants usually caused by nonstandard means of dispersal? Ecology 84, 1945–1956. Hughes, L., Dunlop, M., French, K., Leishman, M.R., Rice, B., Rodgerson, L., Westoby, M., 1994. Predicting dispersal spectra: a minimal set of hypotheses based on plant attributes. J. Ecol. 82, 933–950. Jurado, E., Westoby, M., Nelson, D., 1991. Diaspore weight, dispersal, growth form and perenniality of Central Australian plants. J. Ecol. 80, 416–417. Jurado, E., Estrada, E., Moles, A., 2001. Characterizing plant attributes with particular emphasis on seeds in Tamaulipas thornscrub in semi-arid Mexico. J. Arid Environ. 48, 309–321. Kleyer, M., 1999. Distribution of plant functional types along gradients of disturbance intensity and resource apply in an agricultural landscape. J. Veg. Sci. 10, 697–708. Knevel, I.C., Bekker, R.M., Kunzmann, D., Stadler, M., Thompson, K., 2005. The LEDA Traitbase. Collecting and measuring of life-history traits of the Northwest European Flora. University of Groningen, Community and Conversation Ecology Group, Scholma Druk B.V., Bedum. Ko¨rner, C., 2003. Alpine Plant Life. Functional Plant Ecology of High Mountain Ecosystems, second ed. Springer, Berlin. Lavorel, S., O’Neill, R.V., Gardner, R.H., 1994. Spatiotemporal dispersal strategies and annual plant species coexistence in a structural landscape. Oikos 71, 75–88. Leishman, M.R., Westoby, M., 1994. The role of large seed size in shaded conditions: experimental evidence. Funct. Ecol. 8, 205–214.

ARTICLE IN PRESS 672

T. Navarro et al. / Flora 204 (2009) 658–672

Leishman, M.R., Westoby, M., Jurado, E., 1995. Correlates of seed size variation: a comparison among five temperate floras. J. Ecol. 83, 517–530. Leishman, M.R.W., Moles, A.T., Westoby, M., 2000. The evolutionary ecology of seed size. In: Fenner, M. (Ed.), Seeds: The Ecology of Regeneration in Plant Communities, second ed. CAB International, Wallingford, UK, pp. 31–58. Metcalfe, D.J., Grubb, P.J., 1995. Seed mass and light requirements for regeneration in Southeast Asian rain forest. Can. J. Bot. 73, 817–826. Moles, A.T., Ackerly, D.D., Webb, C.O., Tweddle, J.C., Dickie, J.B., Westoby, M., 2005. A brief history of seed size. Science 307, 576–580. Murbeck, S., 1919. Beitra¨ge zur Biologie der Wu¨stenpflanzen. Vorkommen und Bedeutung von Schleimabsonderung aus Samenhu¨llen, Lunds Universitets Arsskrift. Navarro, T., Nieto-Caldera, J.M., Pe´rez-Latorre, A.V., Cabezudo, B., 1993. Estudios fenomorfolo´gicos en la vegetacio´n del sur de Espan˜a III. Comportamiento estacional de una comunidad de badlands (Tabernas, Almerı´a, Espan˜a). Acta Bot. Malacitana 17, 189–200. Navarro, T., Alados, C.L., Cabezudo, B., 2006. Changes in plant functional types in response to goat and sheep grazing in two semi-arid shrublands of SE Spain. J. Arid Environ. 64, 298–322. Palmer, M.A., Ambrose, R.F., Poff, N.L., 1997. Ecological theory and community restoration ecology. Restor. Ecol. 5, 291–300. Parmesan, C., Yohe, G., 2003. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 37–42. Pa¨rtel, M., Zobel, M., Zobel, K., Van der Maarel, E., 1996. The species pool and its relation to species richness: evidence from Estonian plant communities. Oikos 75, 111–117. Pauli, H., Gottfried, M., Grabherr, G., 2001. High summits of the Alps in a changing climate. The oldest observation series on high mountain plant diversity in Europe. In: Walther, G.H., Burga, C.A., Edwards, P.J. (Eds.), Fingerprints of Climate Change. Adapted Behaviour and Shifting Species Range. Kluwer Academic/Plenum Publishers, New York, pp. 139–149. Puigdefabregas, J., Pugnaire, F.I., 1999. Plant survival in arid environments. In: Pugnaire, F.I., Valladares, F. (Eds.), Handbook of Functional Plant Ecology. Marcel Dekker, New York, pp. 381–407. Que´zel, P., 1952. Contribution a` l’e´tude phytoge´ographique et phytosociologiques du Grand Atlas calcaire. Me´m. Soc. Sci. Nat. Maroc. 50, 1–57. Que´zel, P., 1957. Peuplements ve´ge´taux des hautes montagnes de l’Afrique du Nord. Essai de synthe`se bioge´ographique et phytosociologique. Edit. Lechevalier, Paris, 463pp.

Sarmiento, G., Monasterio, M., 1983. Life-form and phenology. In: Bourliere, F. (Ed.), Ecosystems of the World. Tropical Savannas. Elsevier, Amsterdam, pp. 79–108. Snow, D.W., 1965. A possible selective factor in the evolution of fruiting seasons in tropical forest. Oikos 15, 274–281. Snow, D.W., 1971. Evolutionary aspects of fruit-eating by birds. Ibis 13, 194–202. Sobral Griz, L.M., Machado, I.C., 2001. Fruiting phenology and seed dispersal syndromes in caatinga, a tropical dry forest in the northeast of Brazil. J. Trop. Ecol. 17, 303–321. Taleb, M.S., Fennane, M., 2003. Etude des groupements steppiques du Parc National du Haut Atlas oriental et ses bordures (Maroc). Bull. Inst. Sci. Rabat 25, 25–41. Taleb, M.S., Fennane, M., 2008. Diversite´ du Parc National du Haut Atlas Oriental et des massifs Ayachi et Maaˆsker (Maroc). Acta Bot. Malacitana 33, 125–145. Thompson, K., Rabinowitz, D., 1989. Do big plants have big seeds? Amer. Nat. 133, 722–728. Thompson, K., Bakker, J., Bekker, R.M., Hodgson, J., 1998. Ecological correlates of seed persistence in soil in the northwest European flora. J. Ecol. 86, 163–169. Tiffney, B.H., 1984. Seed size, dispersal syndromes, and the rise of the angiosperms: evidence and hypothesis. Ann. Missouri Bot. Gard. 71, 551–576. Trakhtenbrot, A., Nathan, R., Perry, G., Richardson, D.M., 2005. The importance of long-dispersal in biodiversity conservation. Divers. Distrib. 11, 173–181. Van Rheede van Oudtshoorn, K., Van Rooyen, M.W., 1999. Dispersal Biology of Desert Plants. Springer, New Cork. Van Rooyen, M.W., Theron, G.K., Grobbelaar, N., 1990. Life form and dispersal spectra of the Namaqualand, South Africa. J. Arid Environ. 19, 133–145. Venable, D.L., Levin, D.A., 1985. Ecology of achene dimorphism in Heterotheca latifolia. I. Achene structure, germination and dispersal. J. Ecol. 73, 133–145. Weiher, E., Van der Werf, A., Thompson, K., Roderick, M., Garnier, E., Eriksson, O., 1999. Challenging Theophrastus: A common core list of plant traits for functional ecology. J. Veg. Sci. 10, 609–620. Westoby, M., Leishman, M.R., Lord, J., 1996. Comparative ecology of seed size. Trends Ecol. Evol. 7, 368–372. Willson, M.F., 1993. Dispersal mode, seed shadows, and colonization patterns. Vegetatio 108, 261–280. Willson, M.F., Thompson, J.N., 1982. Phenology and ecology of color in bird-dispersed fruits, or why some fruits are red when they are ‘green’. Can. J. Bot. 60, 701–713. Zhang, S.T., Du, G.Z., Chen, J.K., 2004. Seed size in relation to phylogeny, growth form and longevity in a subalpine meadow on the east of the Tibetan plateau. Folia Geobot. Phytotaxon. 39, 129–142. Zohary, M., 1937. Die verbreitungso¨kologischen Verha¨ltnisse der Pflanzen Pala¨stinas. Beih. Bot. Cent.bl. 56, 1–155. Zohary, M., 1962. Plant Life of Palestine, Israel and Jordan. The Ronald Press, New York.