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Phenomorphology and eco-morphological characters of Rhododendron lauroid

forests in the Western Mediterranean (Iberian Peninsula, Spain)

A.V. Perez Latorre* and B. CabezudoDepartamento de Biologıa Vegetal. Facultad de Ciencias, Universidad de Malaga, Apartado 59, E-29080Malaga, Spain; *Author for correspondence (e-mail: avperez@uma.es; fax: +34 952131944)

Received 2 November 2004; accepted in revised form 25 April 2005

Key words: Functional types, Growth-forms, Phenophasic patterns, Relict, Rhododendron

Abstract

The evergreen broad-leaved forest of Rhododendron ponticum represents a special type of Mediterraneanvegetation because of their relict nature (allegedly pre-glacial, Southern-Iberian and Pontic) and connectionwith Macaronesian-Atlantic flora. The findings of ecomorphological (growth forms) and phenological(phenology) studies point to characteristics typical of its relict character and its relationship with sub-tropical lauroid vegetation (greater forest stratification, larger leaves, high percentage of photosyntheticstems, scarce tomentosity, pre-flowering in a season different to Mediterranean species and closeness ofautumn–winter flowering species). There are, however, links with typical Mediterranean vegetation(Quercus L. forests) that surrounds the Rhododendron stands, due to its adaptation to Mediterraneanclimate (sclerophyll leaves, plant and leaf duration, post-fire regeneration, fleshy fruit and fruit setting-seeddispersal seasonality). Within the community, different groups of plants show different adaptations to thesame biotope, suggesting their distinct paleo-phytogeographical origins. The results confirm the singularityof this vegetation within the typically Mediterranean environment where it grows and its connections withother extra-Mediterranean types.

Introduction

The use of ecomorphology (growth forms) andphenomorphology to study Mediterranean vege-tation and flora was first proposed by Orshan(1982, 1983, 1986 and 1989). Growth forms pro-vide information on adaptive traits (Mooney 1974;Le Roux et al. 1984; Pierce 1984), while a pheno-morphological study provides data on the com-plete annual cycle concerning changes in theorgans in relation to seasonal climatic changes andplant architecture. These methods, which may beincluded in the broad definition of ‘functionaltypes’ (Box 1987), have confirmed excellent forcataloguing vegetation (Nemani and Running1996), relating vegetation with climatic parameters

(Box 1996), predicting its dynamism (Noble andGitay 1996) even detecting species outside theirecological context (Herrera 1984, 1987). In thecase of Mediterranean vegetation, the standardi-sation of methodology not only allows betweenecosystems comparison but also means it can beused for describing as a function of ecomorpho-logical (growth forms) and phenomorphologicalcharacteristics (Floret et al. 1987, 1990). Themethod has been used in Mediterranean regions ofthe world, including Australia (Pate et al. 1984),Chile (Orshan et al. 1984; Montenegro et al.1989), France (Floret et al. 1987, 1990; Romane1987), Israel (Danin and Orshan 1990; Keshetet al. 1990), South Africa (Le Roux et al. 1989)and Spain (Cabezudo et al. 1992, 1993; Perez

Plant Ecology (2006) 187:227–247 � Springer 2006

DOI 10.1007/s11258-005-6574-0

Latorre et al. 1995, 2001; Caritat et al. 1997;Navarro and Cabezudo 1998; Castro Dıez andMontserrat Martı 1998; Perez Latorre and Cab-ezudo 2002). Perez Latorre and Cabezudo (2002)proposed a synthesis of the Orshan’s method to beapplicable to Mediterranean climate regions in theworld. The synthesis was applied to woodlands(Quercus suber L., Fagaceae) and shrublands (Ci-stus L. spp., Cistaceae) in Spain, observing cleardistinctions between the two formations as regardsboth ecomorphological (growth forms) and phe-nological parameters (phenophases and relatedindexes).

Here we continue this line of work by applyingthe method proposed by Perez Latorre and Cab-ezudo (2002) to a type of vegetation of great paleo-phytogeographical and conservation interest: thepaleomediterranean relict lauroid forests of Rho-dodendron ponticum L. (Ericaceae). These datefrom the end of the Tertiary (Quezel 1985; Mai1989) and are now relegated to the extreme en-claves of western (Strait of Gibraltar) to eastern(Bosphorus) Mediterranean, showing climaticpeculiarities in both sites.

The main objective of this work is to characte-rise and describe this kind of plant communityusing ecomorphology and phenomorphology andto study the relationships with the ecologicalparameters of the biotope where it develops. An-other objective is to analyse the standardised datato discuss the originality or similarity of Rhodo-dendron forest to other kind of typically Mediter-ranean forest (Quercus suber). We also try to makean approach to eco-phenomorphological groupingof species following a combination of their eco-morphological and phenophasic patterns. Finally,we try to find characters that support the relictorigin of Rhododendron forests and its eco-phe-nomorphological relations to present lauroid veg-etation.

Methods

Vegetation

The studied vegetation type corresponds to ripar-ian forest dominated by Rhododendron ponticum(Scrophulario laxiflorae–Rhododendretum pontici

Perez Latorre et al. 2000). Called ‘ojaranzal’ inSpanish, this community is uniquely found in SWIberia within western Europe (Spain and Portugal)(Perez Latorre et al. 1996) and belongs to theWestern Mediterranean relict lauroid vegetation(Rhododendretalia pontici Perez Latorre et al.2000, Pruno-Lauretea azoricae Oberdorfer exSunding 1972) (Cabezudo and Perez Latorre2001). In Spain, its most important representativeis found in Andalusia (Los Alcornocales NaturalPark, Cadiz Province; Perez Latorre et al. 1999)while much smaller populations are found in theSierras de Monchique and Vouzela in Portugal(Pereira Dıas and Barros de Sa Nogueira 1973;Malato Beliz 1982). The most unusual floristiccharacteristic of this community is the brio-pte-ridophytic stratum with species which have aMacaronesian-Atlantic optimum or paleomedi-terranean origin (such as Lepidopilum virens Card.,Tetrastichium fontanum (Mitt.) Card., Neckeraintermedia var. laevifolia (Schiffn.) Renauld andCardot, Homalia webbiana Mont., Isopterygiumbottini (Breidl.) Broth-Bryophyta-. Culcita macro-carpa C. Presl., Diplazium caudatum (Cav.) Jer-myPteris incompleta Cav., Vandenboschia speciosa(Willd.) Kunkel -Pteridophyta-) (Salvo 1990; Gu-erra et al. 2003).

Study site

The study site was chosen taking into considerationthe presence of most of the species belonging to thecommunity and the state of conservation. The se-lected R. ponticum stand (Figure 1) lies within aprotected area (Los Alcornocales Natural Park,Los Barrios municipality, Dehesa de Ojen) in theprovince of Cadiz (Spain). The riparian site occu-pies a 10 m wide, 20 m long stretch at 350 m a.s.l.(5�36¢ W/36�7¢ N). A permanent stream flows onsiliceous sands, the bed of which contains largerocky blocks. The soil data (Table 1) point to a lowpH and the absence of carbonates, while climaticdata (Figure 2, Table 2) reveal a typically Medi-terranean warm climate (thermomediterraneanbioclimatic belt with an average annual tempera-ture of 17.6 �C) and much rain (humid ombrotype,average annual rainfall of 1078 mm) although witha dry period between July and August.

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Figure 1. Little rectangle: distribution of Rhododendron ponticum L. in Spain and general view of the study area. Black dot: location of

the selected plot in the Natural Park of ‘Los Alcornocales’ (Sierra de Ojen, Cadiz province). White dots correspond to other

R. ponticum forests (localities taken from (Perez Latorre et al. 1999, 2000).

229

Ecomorphology

For this ecomorphological study, we used themethod standardised by Orshan (1982, 1986),while following the proposal by Orshan (1989) forthe phenological study. A selective plant inventorywas made in the locality, according to the presenceof the most representative species within thecommunity. The plot measured 200 m2, enough toinclude the whole diversity of species. The inven-tory was made following Braun-Blanquet (1979),including environmental data and plant cover ofthe species, which was divided into persistent andnon-persistent (Table 3). Following the recom-mendations of Orshan (1986) we only took intoaccount the persistent or arid-active species (Eve-nari et al. 1975), that is to say, those that bearaerial active shoots throughout the year and whichare therefore adapted to the Mediterraneandrought season. Arid-passive plants such as

ephemerals (terophytes) and ephemeroids (somegeophytes and hemicryptophytes) were not in-cluded in the studies, because their shoots disap-pear during the unfavourable season (Evenariet al. 1975). The ecomorphological characters(growth forms) were determined for each species inthe field. Twenty-eight characters of those pro-posed by Orshan (1986) were studied as well asfruit type (fleshy, dry), as proposed in (Perez La-torre et al. 1995). Afterwards a species/characterdata matrix was made and the percentage ofpresence of each character expression was calcu-lated on the basis of number of species showingthat character (see Appendix A). For the eco-morphological description of the communities andthe subsequent comparison, we used the charactersand indices proposed by Perez Latorre and Cab-ezudo (2002) including Estimated Biomass of theSpecies (EBS) = plant height (m) · crown diam-eter (m) · canopy or branch density (%), andEstimated Biomass of the Community(EBC) = sum of EBS’s of all the species. Figure 3shows the relative flat form of each species and itspositioning into the community structure.

Phenology and phenophasic indices

Data concerning the different reproductive phe-nological phases (flower bud formation, flowering,fruit setting, seed dispersal) and vegetative phe-nological phases (vegetative growth and leafshedding of dolichoblasts and brachyblasts) wererecorded through monthly visits during a completeannual cycle (2002–2003), for each arid-active orpersistent species (Evenari et al. 1975; Orshan1989). Pteridophytes were excluded of calculations

Table 2. Weather station at Los Barrios (Polvorilla), Cadiz

(5�34¢ W/36�15¢ N).

J F M A M J J A S O N D

Mean annual rainfall (mm)

163.5 169.5 104.7 84.7 50.5 14.8 0.9 2.9 27.7 101.8 191.5 165.8

Mean annual temperature (�C)13.2 14.6 15.2 15.9 18.2 21.3 23 22.4 20.8 16.9 15.3 14.3

It (Thermicity index) = 425, lower thermomediterranean bio-

climatic belt with lower humid ombrotype (Rivas Martınez

classification 1987). Mean annual temperature = 17.6 �C.Absolute minimum temperature = 2 �C. Absolute maximum

temperature = 40 �C. Mean annual rainfall = 1078 mm. Days

of rainfall = 61.5.

Table 1. Main soil characteristics in the area of the study site.

Parameter Type/data

Soil type Alfisol

Rock type Siliceous sandstones

pH horizon A (H2O) 5.6

C/N horizon A 15.7

CO3 horizon A 0

pH horizon B (H2O) 4.7

C/N horizon B 11.2

CO3 horizon B 0

0

20

40

60

80

100

120

J F M A M J J A S O N D

Mean annual rainfall(mm)/2

Mean annualtemperature (ºC)

Figure 2. Climatic diagram of the study area.

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because of the lack of standard reproductive phe-nophases. A minimum of 30 individuals of eachspecies were selected and/or marked when possi-ble, while a phenomorphological herbarium(MGC) with representative samples of the phe-nological phases was collected. For each species aphenological calendar was drawn up (see Appen-dix B), excluding uncommon events (Castro Dıezand Montserrat Martı 1998). The frequency ofeach phenophase taking place in each month wascalculated for the set of species. The phenologicalcalendar of each community was constructed as afunction of the seasonality of the following phe-nological phases: flower bud formation, flowering,fruit setting, seed dispersal, vegetative growth andleaf shedding. The descriptions of the species andvegetation using phenophases and phenophasicindices (Active Phenophasic Period of the SpeciesAPS, Active Phenophasic Period of the Commu-nity APC and Index of reproductive/vegetativeActivity of the Species RVA), were made followingthe model of (Perez Latorre and Cabezudo 2002).

Phenophasic patterns of the species were takenfrom the models described by Montenegro et al.(1989: 385) (patterns A, B, C, D, and E), althougha new phenophasic pattern (F) is here proposed todescribe the almost total coincidence of vegetativegrowth with those of flower bud formation andflowering (Figure 4).

Nomenclature

Valdes et al. (1987) and Castroviejo et al. (1986)were used for this work (Valcarcel 2002, for He-dera; Corley and Crundwell 1991, for Bryophyta).

Results

The main ecomorphological and phenomorpho-logical data are indicated in Appendices A and B.As a result, we made the ecomorphological char-acterisation and the phenophasic calendar.

Table 3. A: releve in the study site, total community cover 100%, north facing slope 15�, area: 10· 25 m. Relative cover based on

Braun-Blanquet index (4 = 61–80%, 2 = 21–40%, 1 = 11–20%, + = 1–10%). B: percentage of presence of species in 16 localities

of the distribution area of R. ponticum forests (taken from Perez Latorre et al. 1999, 2000); * = characteristic species of the com-

munity.

A B

Relative cover Presence (%)

Persistent arid-active plants

*Rhododendron ponticum (Ericaceae) 4 100

*Ilex perado var. iberica (Aquifoliaceae) 2 70

*Hedera maderensis subsp. iberica (Araliaceae) 1 90

Quercus canariensis (Fagaceae) 1 75

Smilax aspera (Smilacaceae) 1 60

Ruscus hypophyllum (Ruscaceae) 1 55

*Frangula alnus subsp. baetica (Rhamnaceae) + 85

Ruscus aculeatus (Ruscaceae) + 55

*Laurus nobilis (Lauraceae) + 50

Alnus glutinosa (Betulaceae) + 45

Viburnum tinus (Caprifoliaceae) + 40

Lonicera periclymenum subsp. hispanica (Caprifoliaceae) + 30

Phyllirea latifolia (Oleaceae) + 30

*Diplazium caudatum (Athyriaceae) + 15

*Scrophularia laxiflora (Scrophulariaceae) + 15

*Pteris incompleta (Pteridaceae) + 10

Ephemerals arid-passive plants

Arisarum proboscideum (Araceae) 2 35

Sibthorpia europaea (Scrophulariaceae) + 35

Ranunculus ficaria (Ranunculaceae) + 10

Brio-pteridophytic synusial species

Athyrium filix-femina (Athyriaceae) 1 75

Vandenboschia speciosa (Hymenophyllaceae) 1 10

Davallia canariensis (Davalliaceae) + 25

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Ecomorphological characterisation

Rhododendron ponticum forest: phanerophytic,scarcely spinescent, holoxyle, multi-layered andevergreen community, with a maximum height of22 m. Leaves are shed periodically on averageevery 18 months; the leaves are predominantlysclerophyll, with a 7% degree of tomentosity, andmostly of about 38 cm2 (micro-mesophyll). Theaverage duration of the plants is 34.8 years; mostare adapted to after-fire regeneration by belowground buds pattern. Vegetative growth andflowering mainly occur in spring and fleshy fruitsare predominant.

Phenophasic calendar

For phenophasic calendar see, Figures 2, 5 and 6,and Table 2. Flower buds formation from autumnto spring, thus avoiding maximum temperaturesand the summer rainfall minima; peak flowering inspring with a secondary maximum in autumn,both warm, rainy seasons with many hours ofdaylight; peak of fruit setting in summer, coin-ciding with maximal temperatures and rainfallminima, lasting into autumn with its abundantrainfall and moderate temperatures; abundantseed dispersal in autumn, reaching a maximum inwinter, when temperatures are at their lowest

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Figure 3. Community structure and biotope. The species are represented to scale in two-dimensional forms, according to the eco-

morphological characters of plant height x crown diameter and placed in their most common position in the biotope. Hedera

maderensis climbs on Quercus canariensis trunks whereas Smilax aspera grows into the canopy of Rhododendron-like tall shrubs and

Lonicera hispanica lies on the canopy of Phillyrea-like tall shrubs.

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(though mild), the days are the shortest and rain-fall plentiful; dolichoblast vegetative growthmaximal in spring, coinciding with an increase intemperatures, continued rainfall and moist soils;dolichoblast leaf shedding maximal in summer,coinciding with the highest temperatures andscant, if any, rainfall, although the second peak inwinter coincides with the lowest temperatures andabundant rainfall.

Discussion

The discussion is made following paragraphsdealing with ecomorphological characters, pheno-logical phases, phenophasic indices, phenophasicpatterns and eco-phenomorphological groups.

Ecomorphological characters

For ecomorphological characters see Tables 4 and 5.

Structure of the community and renewal buds

Biotype distribution (based on renewal bud posi-tion) shows that this is a forest dominated byphanerophytes, as occurs in other types of Medi-terranean forests studied (Oberdorfer 1960; Ro-mane 1987; Floret et al. 1990; Danin and Orshan1990; Perez Latorre and Cabezudo 2002). How-ever, the slight difference in stratification of thislauroid type is quite well reflected in the scaleddistribution of biotypes according to plant heights(Figure 3). The first layer of trees (‘roof’) is con-stituted by mesophanerophyte (5 species) belowwhich there is a dense layer of microphanero-phytes (3 species). Three species of vines (onephanerophyte, one amphiphyte and one chamae-phyte) climb between these two layers. At groundlevel and in areas of low luminosity grow crypto-phytes (two species), hemicryptophytes (twospecies) and one of the two amphiphytes, adapted

Figure 4. Phenophasic patterns of the species that represent the

phenophasic sequence and overlapping of growth and flower-

ing. (A) first: growth, second: growth and buds overlapping,

third: flowering. (B) first: growth, second: buds, third: flower-

ing, no overlapping. (C) first: growth, second: buds and growth

overlapping, third: flowering and growth overlapping. (D) first

buds, second: flowering, third: growth, no overlapping. (E) first:

buds, second: flowering and growth overlapping, third: growth.

(F) first: buds and growth overlapping, second: flowering and

growth overlapping. White rectangle = vegetative growth, grey

rectangle = flower bud formation, black rectangle = flower-

ing. Patterns ‘‘A’’ to ‘‘E’’ from Montenegro et al. (1989). Pat-

tern ‘‘F’’ proposed here.

Reproductive Phenological Phases

0102030405060708090

100

E F M A M J J A S O N D

ps%

FBF FWL FS SD

Figure 5. Time curse of the reproductive phenological phases in

the community expressed as the monthly percentage of species

that show each phenophase. Flower bud formation (FBF),

flowering (F), fruit setting (FS) and seed dispersal (SD).

Vegetative Phenological Phases

0102030405060708090

100

E F M A M J J A S O N D

ps%

DVG LSD BVG LSB

Figure 6. Time curse of the vegetative phenological phases in

the community expressed as the monthly percentage of species

that show each phenophase. Dolichoblast vegetative growth

(DVG), leaf shedding dolichoblast (LSD), brachyblast vegeta-

tive growth (BVG) and leaf shedding brachyblast.

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Table 5. Comparison among communities using ecomorphological characters and phenophases. Bold characters are mean differences

(data for Quercus community from Perez Latorre and Cabezudo 2002).

Rhododendron forest Quercus forest

Ecomorphological characters

Renewal buds position diverse micro-mesophanerophytic

Spinescence almost absent absent

Stratification multi-strata multi-strata

Maximum height 20–30 m 20–30 m

Organs shed leaves leaves and branches

Bark consistency smooth > flaky flaky > smooth

Leaf consistency sclerophylly predominant sclerophylly predominant

Tomentosity (%) 7% 33%

Leaf size average (cm2) micromesophyll (38) micromesophyll (28)

Photosynthetic stems (species %) 44% 19%

Life duration leaves average 18 months average 19 months

Life duration plants average 35 years average 40 years

After fire vegetative regeneration present 75% species present

Main season of shoot growth spring bi-multiseasonal

Main flowering season spring-(bi-multiseasonal) spring

Fruit type predominant fleshy fleshy

Biomass estimated 28 18.3

Phenological phases

Flower bud formation autumn–winter–spring winter–spring

Flowering spring–autumn spring

Fruit setting summer–autumn summer–autumn

Seed dispersal autumn autumn–winter

Dolichoblast vegetative growth spring spring–summer

Leaf shedding dolichoblast summer summer

Brachyblast vegetative growth throughout the year brachyblast absent

Leaf shedding brachyblast summer brachyblast absent

Phytosociological class Pruno-Lauretea Quercetea ilicis

Table 4. Some important ecomorphological characters in the studied species.

Ecomorphological character RW OS BC SP LS LT LC LD SO FT sB

Alnus glutinosa mePh L corky no 20–56 no Ma 6–14 D d 50

Diplazium caudatum H L no no >1640 no sE 26–38 E – 2

Frangula alnus baetica mePh L smooth no 20–56 no Ma 6–14 D f 43

Hedera maderensis iberica ePh L papery no 20–56 no sE 26–38 E f 18

Ilex perado iberica mePh L smooth leaves 20–56 no S 14–26 E f 22

Laurus nobilis mePh L smooth no 20–56 no S 26–38 E f 25

Lonicera peryclimenum hispanica Am Bb/L flaky no 20–56 yes Ma <6 D f 3

Phyllirea latifolia miPh L smooth no 12–20 no sE 14–26 E f 8

Pteris incompleta H L no no >1640 no sE 14–26 E – 2

Quercus canariensis mePh L corky no 56–180 no sE 6–14 D f 206

Rhododendron ponticum miPh L flaky no 20–56 no sE 6–14 E d 35

Ruscus aculeatus Cr Sh smooth leaves* 2–12 no S 14–26* E f 0.2

Ruscus hypophyllum Cr Sh smooth leaves* 12–20 no Ma 14–26* E f 1

Scrophularia laxiflora Am Bb/Sh no no 20–56 no Ma <6 E d 0.2

Smilax aspera altissima eCh Bb smooth stems 20–56 no S 14–26 E f 21

Viburnum tinus miPh L smooth no 20–56 no sE 14–26 E f 5

RW = renewal buds position (mePh = mesophanerophyte, miPh = microphanerophyte, ePh = escandent phanerophyte,

Am = amphiphyte, H = hemicryptophyte, Cr = cryptophyte, eCh = escandent chamaephyte). OS = organs shed rhythmically

(Bb = basipetal branch shedders, L = leaves, Sh = shoots). BC = bark consistency. SP = spinescence. LS = dolichoblast leaf

size (cm2). LT = leaf tomentosity. LC = leaf consistency (Ma = malacophyll, sE = semisclerophyll, S = sclerophyll,).

LD = dolichoblast leaf duration (months). SO = seasonality of assimilating organs (E = evergreen, D = deciduous). FT = fruit

type (d = dry, f = fleshy). sB = estimated biomass. * = phylloclades.

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to the light limiting factor. The existence of this‘‘roof’’, which creates a favourable microclimate,is perhaps responsible for the persistence of therest of the substrates. Regardless of the height ofthe phanerophytes, canopy diameters of 2–5 mpredominate, suggesting strong competition forhorizontal space, although the height of Quercuscanariensis Willd. permits it to reach diameters of15 m, while the multi-trunks growth of Rhodo-dendron permits a canopy in excess of 5 m. Can-opy density is generally very high (>75%), whichgradually diminishes the amount of light reachingsuccessive layers, meaning that the understoreymust be composed of shade-tolerant species, withlarge shoots and leaves, maintained by the goodhumidity of the biotope (Smith and Huston 1989).The estimated biomass for this community is 27.6,placing it well above the shrublands of Cistus (0.4)and even Quercus suber forests (18.3) (Perez La-torre and Cabezudo 2002).

Shoots, barks, post-fire regeneration

The community as a whole shows lignified shoots,only the ephemeroids (not included in the study)are axyle (Arisarum Miller, Ranunculus L., etc.).Smooth barks predominate (8 species), unlike intypical Mediterranean woods of Q. suber wherethe predominant type is flaky (Perez Latorre andCabezudo 2002). Only two species (Lonicera hi-spanica and Rhododendron ponticum) show shed-ding barks (which are also flaky) leading to anaccumulation of this inflammable dry material onthe floor. Two species with protective corky bark(Alnus glutinosa and Quercus canariensis) arecapable of post-fire regeneration while most (12species) regenerate by epicormic or rhizome budsbelow ground level. Only ferns, the vine Lonicerapericlymenum subsp. . hispanica (Boiss. and Re-uter) Nyman and the amphiphyte Scrophularialaxiflora Lange die after fire. In this respect, Rho-dodendron forests closely resemble typical Medi-terranean Q. suber forests, although no specieswith aerial regenerating epicormic buds are to befound (Perez Latorre and Cabezudo 2002) forwhich fire would lead to temporary destruction ofcommunity stratification and loss for several yearsof low light conditions necessary for the mainte-nance of relict pteridophytes and bryophytes (Salvo1990; Cabezudo et al. 1995; Guerra et al. 2003).

Photosynthetic organs

One of the most important aspects of the forest isthe leaves area. Large leaves predominate in thecommunity (micro-mesophyll, 20–56 cm2), withthe presence of a very large-leafed species (Quercuscanariensis) with 56–180 cm2 (mesophyll) and twoferns with megaphyll leaves. Such characteristicsdifferentiate this wood even further from theMediterranean Q. suber forest with its predomi-nant leaf size of 2–20 cm2 and where it is alsopossible to find nanophyll-leaved species(<2 cm2). This predominance of large leaves andhigh canopy densities provides strong shade to thelower strata and the ground, almost totallyinhibiting the presence of herbaceous under-growth, but preserves the relict ferns, which wouldotherwise disappear through the photo-destructionof its pigments (Ratcliffe et al. 1993). Only in au-tumn and winter does the intensity of the shadediminish due to the loss of leaves of the threedeciduous species (Q. canariensis, Frangula alnusssp. baetica (Reverchon and Willk.) Rivas Godayex Devesa and Alnus glutinosa (L.) Gaertner). Thebiomass represented by these large leaves ismaintained by the favourable environmental con-ditions of the area with a mean temperature abovethe minimum for vegetative activity, abundantrainfall, mists and high soil humidity levels (Wer-ger and Ellenbroek 1978; Keshet et al. 1990), un-like those found in other Mediterranean woods ofaverage humidity, such as Q. suber forests (PerezLatorre and Cabezudo 2002). The predominanceof large leaves may also be due to the low level ofnutrients in the soil (Givinish 1987) and lentweight by the presence of Alnus, a known nitrogen-fixer. The dense shade may explain the high per-centage of species with photosynthetic stems(44%), three small species (Ruscus L. spp. andScrophularia) which grows in the understorey,Smilax aspera L., which only climbs to interme-diate height levels, and Hedera maderensis ssp.iberica McAllister, whose stems remain below treecanopies. The most interesting case is thatregarding Ilex perado var. iberica Loes. and Laurusnobilis L., both small trees, with their long-lastingphotosynthetic branches (3–5 years) and height ofhalf a metre or more, which have low light andwater requirements corresponding to stress-toler-ant plants (long-lasting aerial parts, sclerophyllleaves, photosynthetic stems) (Grime 1979; Chapin

235

et al. 1993) but which grow in a biotope whichtheoretically provides good year-round conditions.

Leaves morphology

The combination of green and glabrous leaves (15species), without defence against dry conditionssuch as hairs and resins would provide (Oppenhei-mer 1960), and horizontally inserted leaves (12species) predominates, which, together with thelarge areas of the leaves, produces a very attenuatedlight in intermediate and low layers of the vegetationand produces a humid biotope (Keshet et al. 1990).The glabrous leaves with some sclerophyll degreeare in contrast with the malacophyll-glabrouscombination typical of Mediterranean shrublands(Perez Latorre and Cabezudo 2002). A group ofmalacophyll-glabrous plants (Alnus and Frangula)corresponds to winter-deciduous species whoseleaves last less than 1 year. Sclerophyll leaf impliesadaptation to water stress (Parsons 1976; Campbelland Cowling 1985; Givinish 1987) and is thereforesomewhat surprising in these conditionswhere thereis no lack of water (Grieve 1953). However, it isprobably the result of the pre-Mediterranean originof the concerned species and their relict status(Axelrod 1975; Herrera 1984). Even it may reflect‘ghost’ paleoclimatic conditions different from thepresent day (Went 1971) or simply is the result of thenutrient-poor soils (Table 1) (Mooney et al. 1983)(with Alnus as a nitrogen-fixer) typical of tropicalwoods (Larcher 1977)withwhichR. ponticum forestmay be ecomorphologically related.

Spinescence is unusual in the forest, as it is inother humid Mediterranean woods (Perez Latorreand Cabezudo 2002) and, curiously, only appearson leaves or phylloclades (Smilax, not always, Ilex,not always, and Ruscus spp.) and not on stems.Long-lasting (2 or 3 years) leaves predominate, acharacteristic positively associated with increasedrainfall (Keshet et al. 1990) in Mediterraneanvegetation (Orshan 1982), conferring an evergreenappearance to the community, except in the case ofthe small group of winter-deciduous and malaco-phyll species (Alnus, Frangula, Quercus, Lonicera)whose leaves last less than a year and whichprobably have an origin, as floristic contingent,different to the sclerophyll evergreen species(which, nevertheless, partially lose their leaves insummer). The phanerophytes/chamaephytes index

(Danin and Orshan 1990) points to the totalinhibition of the latter due to the conditions im-posed by the dense forest, except for the climberchamaephyte Smilax.

Seasonality, fruits

Rhododendron forest is an evergreen community,reflecting mature Mediterranean formations ofsucesional stages. However, there is a deciduouscontingent of three species (Alnus glutinosa, Fran-gula alnus subsp. baetica, Quercus canariensis)which points to a certain degree of coldness andhumidity (Keshet et al. 1990), the first of which nolonger applies, so that Alnus and Frangula, at least,probably come from a floristic contingent (Euro-Siberian), a relict of cold periglacial eras. Thecommunity is characterised by plants (10 species)with a predominantly spring growth pattern andwhich include the deciduous plants, and anothersix species showing multi-seasonal growth (ever-greens). Growth stops from mid-summer to mid-winter, which does not reflect the good prevailinghydric and climatic characteristics (Table 2). Thisdisagreement reinforces the possibility of an originin differently-adapted floras. The flowering seasonunderlines this contradiction, since although typi-cal Mediterranean spring flowering predominates(6 species), two species (Alnus, Viburnum tinus L.)flower in winter and two (Hedera, Smilax, climb-ers) in autumn (Herrera 1984). The species show-ing multi-seasonal flowering or spores dispersalare, curiously, relict ferns and Ruscus ssp. Thefleshy fruits are characteristic of other Mediterra-nean woods (Perez Latorre and Cabezudo 2002)and point to the summer availability of groundwater, which disagrees with the typical and almosttotal absence of summer rains.

Phenological phases

For phenological phases see Figure 5, 6 and 7 andTable 5.

Flower buds formation

This phenophase is maintained throughout theyear, with minimum levels in summer and maxi-mum in September, unlike in woods of Quercus

236

suber, when the maximum occurs in February–March. Such long periods (lasting more than5 months) are frequent, sometimes preceding ashort flowering period (Alnus, Rhododendron,Viburnum) and sometimes lasting the whole year(Ruscus); while in the case of Laurus nobilis it isdue to two flowerings, one in spring and one inautumn. The shortest period (1 month) occurs inQuercus canariensis.

Flowering

Maximum flowering occurs in spring, reducing toalmost zero in summer, the least favourable sea-son, and with a significant secondary peak in au-tumn. Spring flowering species include Frangulabaetica, Quercus canariensis, Rhododendron ponti-cum and Ilex perado. Those flowering in autumnare Hedera maderensis and Smilax aspera, whileLaurus nobilis flowers in both spring and autumn,although no fruits appear in the latter. Alnus glu-tinosa and Viburnum tinus flower in winter, whileboth species of Ruscus flower practically the wholeyear, except in the middle of summer. Phillyrealatifolia L. did not flower during the study period,as occurred in the study of a subhumid Mediter-ranean wood of Quercus suber (Perez Latorre andCabezudo 2002), perhaps due to an excess of shade(Sack et al. 2003). The combination of differentflowering periods and a secondary peak in autumnare similar to those detected by Perez Latorre andCabezudo (op. cit.). The pteridophytes (Diplazium,Pteris) sporulated throughout the year.

Fruit setting

Fructification begins in spring and is at a heightthroughout the summer, with a secondary peak inautumn and a minimum in winter, as similar to thepattern of Quercus suber woods observed by PerezLatorre and Cabezudo (2002). Since most are fle-shy fruit, it is not surprising that fructification lastsuntil autumn. The longest fruiting period is that ofIlex perado and Laurus nobilis (8 months) and theshortest occurs in Frangula, Smilax and Lonicera(2 months, despite the fleshy nature of the fruit).Both species of Ruscus bear fruit throughout theyear, the result of several flowerings and supportedby the permanent shaded conditions (Sack et al.

2003), although few individuals of the respectivepopulations do so at a time.

Seed dispersal

Dispersion shows two maxima, in autumn andwinter, with a minimum as spring turns to sum-mer, at which time other antagonist phenophase(flowering) is at its height, as occurs in Mediter-ranean woods of Quercus suber (Perez Latorre andCabezudo 2002). Summer dispersing species areScrophularia laxiflora (dry fruit/nuts) and Lonicerahispanica, while Ruscus spp. disperses its fruitsthroughout the year, although always in isolatedindividuals. The longest seed dispersal period isthat shown by Alnus, Ilex and Viburnum, whichmaintain mature fruit on their branches for up to6 months.

Leaf shedding

Leaf shedding is maximal in summer, coincidingwith the dry period and decrease in the water levelof the stream, which is typical of evergreen speciessuffering a facultative and partial loss of dolicho-blast leaves. A second maximum occurs at thebeginning of winter due to the presence of decid-uous species (Frangula, Quercus, Alnus) the firstcontinuing to shed leaves until the followingspring. Neither Ruscus spp. nor Smilax shed theirleaves (phylloclades in the former) since thebranches are completely renewed. Quercus canari-ensis does not shed all of its leaves but maintains asmall percentage even at the beginning of spring,when the new branches are formed, behavioursimilar to that recorded for Quercus faginea ssp.broteroi (Cout.) A. Camus in Quercus suber woods(Perez Latorre and Cabezudo, 2002). This may bethe result of the favourable climatic conditions ofthe study area.

Vegetative growth

Vegetative growth is maximal during the springand is zero in August, September and October,unlike in other Mediterranean woods (Perez La-torre and Cabezudo 2002) where the growth, al-though low, continues in these months. No species

237

continues growing throughout the year, which isperhaps surprising, given that the climatic (seeFigure 2 and Table 2) and soil (permanent riparianwater) conditions are suitable for a year-roundgrowth. However, there are partial flower budsformation and fructification peaks, which pre-sumably compete for the resources necessary forgrowth (Castro Dıez et al. 2003). Some species dokeep growing for several months (7–9 months inthe case of Scrophularia, Hedera and Pteris), whileDiplazium is the only species that continues to growthroughout the year. The shortest growth period isthat of Frangula, Quercus, Rhododendron, Ilex andPhillyrea, which all last for 2 months or less. Theaccumulation of dead matter on the plants (bran-ches, inflorescences, etc.) is greatest in spring (80%)and least in autumn (35%) (Figure 7).

Phenophasic indices

For phenophasic indices see Appendix B. TheActive Phenophasic Period of Species (APS),which indicates the number of months withfavourable conditions for reproductive activityand growth, points to three phenomorphologi-cal patterns in the community. A very hetero-geneous group making up the majority ofspecies and representative of the communityshows activity practically throughout the year.These are Alnus, Hedera, Ilex, Laurus, Lonicera,Scrophularia, Rhododendron, Ruscus, Viburnumand the pteridophytes Diplazium and Pteris.Another group shows activity during 8–9 months (Quercus, Smilax), while Frangula al-nus concentrates its activity into 4 months. Ofspecial interest is Phillyrea, in whose adultpopulation no reproductive phenophasic activitywas detected, probably because of the above-

mentioned reasons. (Perez Latorre and Cab-ezudo 2002) also identified three groups inMediterranean Q. suber woods, although lessheterogeneous in their case.

As regards the Active Phenophasic Period ofthe Community (APC) (Figure 8), which indi-cates the percentage of active species (in the senseof APS) for each month during the year, thecommunity as a whole shows phenophasic activ-ity between 60 and 100% of the year, but with aspring maximum and winter minimum, with asmall burst during autumn. This pattern showsthat, despite the good conditions of the biotopeas regards temperature and humidity, winterslows down the biomass-forming and reproduc-tive activity. In comparison, Mediterraneanwoods of Quercus suber showed a slightly higheractivity in winter, summer and autumn thanRhododendron forest although both winter andsummer conditions are worse than in our studyarea. The community under study only showed aslightly higher APS in spring. However, theoverall curve obtained for the APS is almostidentical for both the Rhododendron forest andQuercus suber wood.

The Index of reproductive/vegetative Activity ofthe Species (RVA) (Table 6) gives an idea of thedifferent strategies with respect to the time andresources spent in a balance between reproductiveand vegetative phenological phases. Most of theplants (12 species), including all the trees andshrubs, are above 1, indicating the predominanceof reproductive over vegetative phenophases. Themaximum was obtained by Rhododendron with 6and Ilex with 5.5. Four species (all climbers) scoreless than 1, the minimum (0.33) belonging tothe amphiphyte of the understorey Scrophularia

Active Phenophasic Period of Community (APC)

0102030405060708090

100

E F M A M J J A S O N D

ps%

Rhododendron forest Quercus suber forest

Figure 8. Time curse of the APC index (monthly percentage of

species that show phenophasic activity). Comparison between

Rhododendron and Quercus suber communities.

Dead Matter

0102030405060708090

100

E F M A M J J A S O N D

%ps

DM

Figure 7. Time curse of the presence of dead matter on the

plants shoots.

238

laxiflora, which shows a predominance of vegeta-tive over reproductive phenophases. Similar pat-terns were obtained by (Perez Latorre andCabezudo 2002) in Quercus suber woods, where allthe trees and shrubs scored above 1, except someshrubs (Cytisus L.,Genista L.) and Erica arborea L.

Phenophasic patterns

The species of the community can be grouped asfollows (see Figures 4 and 9): no species havepattern A; pattern B is showed by the threeclimbers of the community (Hedera, Lonicera andSmilax); pattern C (flower buds formation andflowering coinciding) corresponds to the onlyamphiphyte (Scrophularia); pattern D (Phillyreaand Rhododendron); pattern E, major species (Al-nus, Ilex, Laurus, Ruscus spp. and Viburnum);pattern F is for deciduous trees (Frangula andQuercus). Grouping these patterns into two basictypes, the species can be divided into: (a) the fivespecies that grow first and then flower(A + B + D) and (b) those that grow and flowerat the same time (C + E + F) (9 species). Similarphenophasic patterns were seen in the Mediterra-nean wood of Quercus suber (Perez Latorre andCabezudo 2002). There were no significant differ-ences between the communities as regards patternsB, D, E and F, although the first three parameterswere slightly higher in the Rhododendron forest

and F was higher in the Q. suber wood. Pattern Cis much less common in the Rhododendron forest.

Eco-phenomorphological groups

It is possible to create a series of eco-phenomor-phological groups in communities by combining thephenophasic behaviour of the species and given eco-morphological characters. In this way, groups withdifferent adaptations and behaviour can be identi-fied in the same biotope and within the same com-munity (Perez Latorre and Cabezudo 2002). Sevensuch groups appear in the Rhododendron forest (seeTable 7) as a function of the main flowering/sporesdispersal season, phenophasic pattern and biologi-cal type (plant size) plus seasonality and leaf con-sistency. The result is somewhat surprising since theresponse of the vegetation to such a homogeneousbiotope with so few species shows very differentphenophasic and ecomorphological adaptations,which might suggest different contingents of plantsadapted to the biotope over a long period of time(Herrera 1984). The only strictly winter-floweringspecies are Alnus and Viburnum, which show a verysimilar phenophasic calendar and identical pattern,but very different biological types and leaves. Thespring-flowering species, Frangula and Quercus,show almost identical calendar and pattern, differ-entiating themselves from the following group in

Phenophasic patterns

0

5

10

15

20

25

30

35

40

45

A B C D E F

iceps

% se

Rhododendron forest Quercus suber forest

Figure 9 Percentage of species presenting each phenophasic

pattern (A–F). Comparison between R. ponticum forest and

Quercus suber forest.

Table 6. RVA index and phenophasic patterns of the species of

the community.

Species RVA Phenophasic patterns

Scrophularia laxiflora 0,33 C

Lonicera peryclimenum hispanica 0,5 B

Smilax aspera altissima 0,8 B

Hedera maderensis iberica 0,86 B

Frangula alnus baetica 2 F

Ruscus hypophyllum 2 E

Viburnum tinus 2,2 E

Ruscus aculeatus 2,4 E

Alnus glutinosa 3 E

Laurus nobilis 4 E

Quercus canariensis 4 F

Ilex perado iberica 5,5 E

Rhododendron ponticum 6 D

Phyllirea latifolia – D

239

that they are deciduous. Ilex, Laurus and Rhodo-dendron are also very similar, including theireco-morphological traits (especially of the leaves),although the first show an E pattern and the third aD type. With autumnal flowering, Hedera andSmilax show almost identical calendars and phe-nophasic patterns but differ in their architecture andecomorphology. The only species that flower insummer are Lonicera and Scrophularia, with verysimilar calendar but different patterns and biologi-cal types. The two species of Ruscus are, unsur-prisingly, very similar, with multi-seasonalreproductive phenophases.Phillyrea distances itselffrom all the plants of the forest because of its lack ofa reproductive phenophase, but is included in thegroup of Rhododendron because of its vegetativephenophases, phenophasic pattern and biologicaltype.Diplazium and Pteris are grouped together, asis to be expected, because of the level of theirpteridophytic form and multi-seasonal spores dis-persal (reproduction).

Conclusions

Similarities between Rhododendron forests andQuercus suber woods are phenologically reflected(Table 5) in fruit setting, seed dispersal, APS andphenophasic patterns. As regards common eco-morphological traits, the most important aspectsare the almost complete absence of spinescence,

maximum trees height, sclerophylly, leaf and plantduration, after-fire vegetative regeneration and fle-shy fruits.

Among the differential features (Table 5) are thegreater number of layers in Rhododendron forest,the greater amount of estimated biomass, thepredominance of smooth over flaky barks, thegreater leaf size (micro-mesophyll), the higherpercentage of photosynthetic stems and lessmarked tomentosity. Phenologically, a differenti-ating character is the maximum flower buds for-mation that is reached at the beginning of autumnand which lasts throughout the year, the fourspecies (25% of the total) that flower in autumn/winter and the low prevalence of the C-type phe-nophasic pattern (flower bud formation andflowering during the last stage of growth).

The relict status of Rhododendron forest can beattributed to several factors that contrast with theprevailing Mediterranean macroclimate, such asthe good conditions that prevail in riparian bio-topes throughout the year. Stress tolerance char-acteristics, such as sclerophylly, are to be found,which may have three possible explanations: (a) thepoor quality and low pH of the soils, (b) adaptationto water stress and (c) the possibility that thecommunity originated from an ancient subtropicalvegetation during the Tertiary. The phenologyfollows seasonal Mediterranean rhythms and doesnot reflect the good conditions which last

Table 7. Grouping of species according to similarity of phenology and selected ecomorphological characters (renewal buds position,

type of fruit, seasonality, spinescence and presence of leaves).

Species FBF F FS SD DVG LSD PPT

Alnus glutinosa UA W SU AW S AW E Mesophanerophyte malacophyll deciduous tree

Viburnum tinus AW W SU AW WS U E Microphanerophyte semisclerophyll evergreen tall shrub

Frangula alnus baetica S S U UA S AWS F Mesophanerophyte malacophyll deciduous tree

Quercus canariensis S S UA AW S W F Mesophanerophyte semisclerophyll deciduous tree

Ilex perado iberica S S UA AW S SU E Mesophanerophyte sclerophyll evergreen tree

Laurus nobilis AWS S SUA A S U E Mesophanerophyte sclerophyll evergreen tree

Rhododendron ponticum AWS S UA AW SU U D Microphanerophyte semisclerophyll evergreen tall shrub

Phillyrea latifolia – – – – S S D Microphanerophyte semisclerophyll evergreen tall shrub

Hedera helix U A A W WSU U B Scandent phanerophyte semisclerophyll evergreen

Smilax mauritanica altissima UA A A W SU – B Scandent chamaephyte sclerophyll evergreen

Lonicera peryclimenum hispanica SU U U U S U B Scandent phanero-chamaephyte malacophyll deciduous

Scrophularia laxiflora S SU U UA WS – C Hemi-chamaephyte malacophyll evergreen herb

Ruscus aculeatus AWS AWS year year S – E Cryptophyte sclerophyll evergreen small shrub

Ruscus hypophyllum UAW AWS year year SU – E Cryptophyte malacophyll evergreen small shrub

Diplazium caudatum – year – – year – – Hemicryptophyte pteridophyte fern

Pteris incompleta – year – – WS – – Hemicryptophyte pteridophyte fern

FBF: flower bud formation, F: flowering, FS: fruit setting, SD: seed dispersal, DVG: dolichoblast vegetative growth, LSD: leaf

shedding dolichoblast, PPT: phenophasic pattern. Bold letters indicate common or unique differential characters of the groups.

Seasons: W = winter, S = spring, U = summer and A = autumn.

240

throughout the year, since, given these, vegetativeand flowering activity might be expected through-out the year, which is not the case (zero DVG inAugust, September and October; minimumAPC inwinter). It is possible that this discordance betweenadaptation and biotope conditions is due to anadaptation to longer cycles (several years) ofdrought, during which the stream would dry upcompletely, creating conditions similar to thosethat would arise from the absence of rainfall.Lastly, the combination of evergreen-sclerophyllleaves, average to large seeds, zoochory dispersion(fleshy fruit) and late sucesional stages points to aflora derived from tertiary-type paleotropical con-ditions (Herrera 1982, 1984; Axelrod 1975).

The paleotropical relict origin of this commu-nity may be supported by the discordance be-tween the adaptive significance of the charactersstudied and the biotope where they occur, con-stituting a good criterion (besides floristic singu-larity in the bryo-pteridophytic stratum) forecosystem conservation under EEC Directive 92/43 referring to EU ‘‘habitats’’ and as SpecialConservation Area of the future European Nat-ure Network 2000.

In the Pontic area (eastern Mediterranean)Rhododendron occurs as understorey of temperatedeciduous forests of Fagus orientalis (Filibecket al. 2004) while in the Iberian Peninsula Rhodo-dendron grows in Mediterranean relict lauroidforests as this work points out. This is a thought-provoking point for future investigations, but wewill not get out of the impasse until we gain pal-aeobotanical information, almost completelylacking at the present day.

Other paths for further investigation may beproposed such as the eco-physiology of relic fernslinked exclusively to the extreme ambient of shadeand phenological calendar of this kind of forest.Studies on functional and taxonomical relation-ships of the mediterranean species of the generaFrangula, Ilex and Laurus to their Macaronesianrelated species will add information about theorigin of this Rhododendron forests. Remains apalaeobotanical mystery, up to date, the absenceof R. ponticum in the north of Morocco, fewkilometres far from the Spanish Rhododendronforests. Effects of climate change in this fragilewater-dependant ecosystems is other avenue offuture research. Finally, phytosociological com-parisons between the Rhododendron Iberian forests

and those of Bulgaria (Strandzja) may clarify thecommon origin of this kind of relic paleomediter-ranean vegetation.

Acknowledgements

Project REN 2000-1155 GLO (C.A.I.C.Y.T.,Spain) ‘‘Diversidad vegetal, ecologıa y estructurade los bosques lauroides relıcticos del sur de laPenınsula Iberica: fitocenosis, especies crıticas,variabilidad genetica de poblaciones y conserva-cion’’ has supported the studies. Dr. J. Carrionfrom the University of Murcia (Spain) and anon-ymous referees have made some valuable sugges-tions on the manuscript.

Appendix A.

Appendix A.

Plants % of

plants

Renewal bud:

mesophanerophyte

5 31

Renewal bud:

microphanerophyte

3 19

Renewal bud:

escandent

phanerophyte

1 6

Renewal bud:

hemicryptophyte

2 13

Renewal bud:

amphiphyte

2 13

Renewal bud:

cryptophyte

2 13

Renewal bud:

chamaephyte

1 6

Organs shed:

leaves

11 69

Organs shed:

amphiphyte

2 13

Organs shed:

shoots

2 13

Organs shed:

branches basipetal

1 6

Plant height:

50–100 cm

3 19

Plant height:

senseless

3 19

Plant height: 5–10 m 3 19

Plant height: 1–2 m 2 13

Plant height: 2–5 m 2 13

Plant height: 10–20 m 2 13

241

Appendix A. Continued.

Plants % of

plants

Plant height: 20–30 m 1 6

Crown diameter: 2–5 m 6 38

Crown diameter: 1–2 m 3 19

Crown diameter: senseless 3 19

Crown diameter: 50–100 cm 1 6

Crown diameter: 25–50 cm 1 6

Crown diameter: 5–10 m 1 6

Crown diameter: >10 m 1 6

Canopy density: 75–90% 5 31

Canopy density: >90 % 4 25

Canopy density: 50–75% 4 25

Canopy density: 25–50% 3 19

Stem consistency: holoxyle 15 94

Stem consistency: hemixyle 1 6

Bark consistency: smooth 7 44

Bark consistency: none 4 25

Bark consistency: flaky 2 13

Bark consistency: corky 2 13

Bark consistency: papery 1 6

Bark thickness <2 14 88

Bark thickness 10–20 mm 1 6

Bark thickness 20–50 cm 1 6

Bark shedding rhythm none 14 88

Bark shedding rhythm 2–5 years 1 6

Bark shedding rhythm >5 years 1 6

Spinescence absent 13 81

Spinescence leaves 2 13

Spinescence stems 1 6

Size larger leaves 20–56 cm2 10 63

Size larger leaves >1640 cm2 2 13

Size larger leaves 12–20 cm2 2 13

Size larger leaves 56–180 cm2 1 6

Size larger leaves 2–12 cm2 1 6

Size smaller leaves: no leaves 15 94

Size smaller leaves <0.2–2 cm2 1 6

Length of larger leaves 5–10 10 63

Length of larger leaves >50 cm 2 13

Length of larger leaves 2–5 2 13

Length of larger leaves 10–20 2 13

Length of smaller leaves: no sm. leaves 15 94

Length of smaller leaves 2–5 1 6

Length of photosynthetic stems:

no phot. stems

9 56

Length of photosynthetic stems

>50 cm

5 31

Length of photosynthetic stems 20–50 2 13

Width of larger leaves 20–50 11 69

Width of larger leaves: >50 cm 5 31

Width of smaller leaves: no sm. leaves 15 94

Width of smaller leaves 5–10 mm 1 6

Width of photosynthetic stems: no phot. stems 9 56

Width of photosynthetic stems 2–3 mm 4 25

Width of photosynthetic stems 3–5 mm 2 13

Width of photosynthetic stems 5–10 1 6

Leaf colour: all green 15 94

Leaf colour green and glaucous 1 6

Appendix A. Continued.

Plants % of

plants

Leaf angle mainly horizontal 12 75

Leaf angle mainly vertical 2 13

Leaf angle all transitions 2 13

Leaf tomentosity: non tomentose 15 94

Leaf tomentosity lower side 1 6

Leaf consistency: semi–sclerophyll 7 44

Leaf consistency malacophyll 5 31

Leaf consistency sclerophyll 4 25

Surface resins absent 16 100

Ratio leaves/assimilating stems: all assim.

leaves

9 56

Ratio leaves/assimilating stems: leaves >

stems

6 38

Ratio leaves/assimilating stems: leaves

aprox. = stems

1 6

Life duration of plant 2–5 years 2 13

Life duration of plant 5–25 years 5 31

Life duration of plant 25–50 years 6 38

Life duration of plant 50–100 years 2 13

Life duration of plant >100 years 1 6

Life duration larger leaves 14–26 months 7 44

Life duration larger leaves 6–14 months 4 25

Life duration larger leaves <6 months 2 13

Life duration larger leaves 26–38 months 3 19

Life duration smaller leaves: no sm. leaves 15 94

Life duration smaller leaves: <6 months 1 6

Life duration assimilating stems: no ass. stems 9 56

Life duration assimilating stems 1–2 years 2 13

Life duration assimilating stems 2–3 years 2 13

Life duration assimilating stems 3–5 years 3 19

Seasonality of assimilating organs evergreen 12 75

Seasonality of assimilating organs winter

deciduous

3 19

Seasonality of assimilating organs summer

deciduous

1 6

Main season of shoot growth spring 10 63

Main season of shoot growth bi-multisea-

sonal

6 38

Main flowering season spring 6 38

Main flowering season bi-multiseasonal 4 25

Main flowering season autumn 2 13

Main flowering season winter 2 13

Main flowering season summer 1 6

Main flowering season: no flowering 1 6

Vegetative regeneration after fire plant killed 4 25

Vegetative regeneration after fire below

ground buds

8 50

Vegetative regeneration below ground non

epicormic buds

4 25

Trophic types autotrophic only 15 94

Trophic types N fixing 1 6

Fruit type: fleshy or fleshy cotyledons 11 69

Fruit type: dry 3 19

Fruit type: no fruits 2 13

242

Appendix B.

243

Appendix B. Continued.

244

Appendix B. Continued.

245

References

Axelrod D.L. 1975. Evolution and biogeography of the Mad-

rean-Tethyan sclerophyll vegetation. Ann. Mo. Bot. Gard.

62: 284–334.

Box E.O. 1987. Plant life forms and Mediterranean environ-

ments. Ann. Bot. 45(2): 7–42.

Box E.O. 1996. Plant functional types and climate at the global

scale. J. Veg. Sci. 7: 309–320.

Braun-Blanquet J. 1979. Fitosociologıa. Bases para el estudio

de las comunidades vegetales. Ed. Blume. Madrid.

Cabezudo B., Navarro T., Perez Latorre A.V., Nieto Caldera

J.M. and Orshan G. 1992. Estudios fenomorfologicos en la

vegetacion del sur de Espana. I. Cistus. Acta Bot. Malacitana

17: 229–237.

Cabezudo B., Perez Latorre A.V., Navarro T. and Nieto Caldera

J.M. 1993. Estudios fenomorfologicos en la vegetacion del sur

de Espana. II. Alcornocales mesomediterraneos (Montes de

Malaga, Malaga). Acta Bot. Malacitana 18: 179–188.

Cabezudo B., Perez Latorre A.V. and Nieto Caldera J.M. 1995.

Regeneracion de un alcornocal incendiado en el sur de

Espana (Istan, Malaga). Acta Bot. Malacitana 20: 143–151.

Cabezudo B. and Perez Latorre A.V. 2001. Notas sobre la

vegetacion de Andalucıa. III. Acta Botanica Malacitana 26:

225–228.

Campbell B.M. and Cowling R.M. 1985. Relationships between

vegetation structure and the environment in the Cape,

Southern Africa: a review. Ann. Bot. 43: 245–255.

Caritat A., Perez Latorre A.V. and Romo A. 1997. The dis-

tribution of ecomorphological types as related to altitude in

the Montseny mountain range (NE Spain). A preliminary

study. Sci. Gerunden. 23: 63–71.

Castro Dıez P. and Montserrat Martı G. 1998. Phenological

pattern of fifteen Mediterranean phanaerophytes from

Quercus ilex communities of NE Spain. Plant Ecol. 139: 103–

112.

Castro Dıez P., Monserrat Martı G. and Cornelissen J.H.C.

2003. Trade-offs between phenology, relative growth rate, life

form and seed mass among 22 Mediterranean woody species.

Plant Ecol. 166: 117–129.

Castroviejo S. et al (eds) 1986. Flora Iberica: Plantas Vasculares

de la Penınsula Iberica e Islas Baleares. Vols. I-XIV. CSIC,

Madrid.

Chapin F.S., Autumn K. and Pugnaire F. 1993. Evolution of

suites of traits in response to environmental stress. Am. Nat.

142: S78–S92.

Chapin F.S., Bret-Harte M.S., Hobbie S.E. and Zong H. 1996.

Plant functional types as predictors of transient responses of

arctic vegetation to global change. J. Veg. Sci. 7: 347–358.

Corley M.F.V. and Crundwell A.C. 1991. Additions and

amendments to the mosses of Europe and the Azores. J.

Bryol. 16: 337–356.

Danin A. and Orshan G. 1990. The distribution of Raunkiaer

life forms in Israel in relation to the environment. J. Veg. Sci.

1: 41–48.

Evenari M.E., Schulze D., Kappen L., Buschbom U. and Lange

O.L. 1975. Adaptive mechanisms in desert plants. In: Vern-

berg E.J. (ed.), Physiological Adaptation to the Environment.

American Institute of Biological Sciences, New York, pp.

111–129.

Filibeck G., Arrigoni P.V. and Blasi C. 2004. Some phytogeo-

graphical remarks on the forest vegetation of Colchis (Wes-

tern Georggia). Webbia 59(1): 189–214.

Floret C., Galan M.J., Le Floc’h E., Orshan G. and Romane F.

1987. Growth form as a tool in characterising vegetation of

small areas. A trial in a Mediterranean environment. Vege-

tatio 71: 3–11.

Floret C., Galan M.J., Le Floc’h E., Orshan G. and Romane F.

1990. Growth forms and phenomorphology traits along an

environmental gradient: tools for studying vegetation? J. Veg.

Sci. 1: 71–80.

Givinish T.J. 1987. Comparative studies of leaf form: assessing

the relative role of selective pressures and phylogenetic con-

straints. New Phytol. (Suppl.) 106: 131–160.

Grieve B.J. 1953. The physiology of sclerophyll plants. J. Roy.

Soc. West Aust. 39: 31–45.

Grime J.P. 1979. Plant Strategies and Vegetation Processes.

Wiley, Chichester.

Guerra J., Cano M.J., Perez Latorre A.V., Ros R.M. and

Cabezudo B. 2003. Flora brio-pteridofıtica de los bosques

lauroides de Rhododendron ponticum L. del Parque Natural

de Los Alcornocales (Cadiz-Malaga, Espana). Acta Bot.

Malacitana 28: 19–36.

Herrera C. 1982. Biologıa reproductiva de plantas lenosas

mediterraneas: sındromes tropicales lejos del tropico. II Jor-

nadas de Taxonomıa Vegetal. Resumen de conferencia,

Sevilla.

Herrera C. 1984. Patrones morfologicos y funcionales en

plantas del matorral mediterraneo del sur de Espana. Stud.

Oecol. 5: 7–34.

Herrera J. 1987. Flower and fruit biology in southern Spanish

mediterranean shrublands. Ann. Mo. Bot. Gard. 74: 69–78.

Keshet M.A., Danin A. and Orshan G. 1990. Distribution of

ecomorphological types along environmental gradients in

Israel: 1. Renewal bud location and leaf attributes. Ecol.

Mediterranea 16: 151–161.

Larcher W. 1977. Ecofisiologıa Vegetal. Ed. Omega, Barcelona.

Le Roux A., Kyriacou X.L. and Orshan G. 1984. The pheno-

morphology of selected plants in Mediterranean-type eco-

systems of South Africa. Bulletin de la Societe Botanique de

France (Actualites Botaniques) 131: 441–450.

Le Roux A., Perry P. and Kyriacou X. 1989. South Africa. In:

Orshan G. (ed.), Plant Phenomorphological Studies in

Mediterranean Type Ecosystems. Kluwer Academic Pub-

lishers, Dodrecht, pp. 159–346.

Mai H.D. 1989. Development and regional differentiation of

the European vegetation during the Tertiary. Plant Syst.

Evol. 162: 79–91.

Malato Beliz J. 1982. A Serra de Monchique. Flora e Vegeta-

cao. Servico Nacional de Parques, Reservas e Patrimonio

Paisagıstico. Lisboa.

Montenegro G., Avila G., Aljaro M.E., Osorio R. and Gomez

M. 1989. Chile. In: Orshan G. (ed.), in Plant Phenomor-

phological Studies in Mediterranean Type Ecosystems. Klu-

wer Academic Publishers, Dodrecht, pp. 347–387.

Mooney H.A. 1974. Plant form as related to environment. In:

Tux en R. (ed.), Handbook of Vegetation Science IV. W.

Junk Den Haag.

Mooney H.A. 1983. Plant form and function in relation to

nutrient gradients. In: Day J.A. (ed.), Mineral Nutrients in

246

Mediterranean Ecosystems. South African Nature Scientist

Programmes Report 71: 55–76.

Navarro T., Nieto Caldera J.M., Perez Latorre A.V. and

Cabezudo B. 1994. Estudios fenomorfologicos en la vegeta-

cion del sur de Espana. III. Comportamiento estacional de

una comunidad de badlands. Acta Bot. Malacitana 18: 189–

198.

Navarro T. and Cabezudo B. 1998. Estrategias fenomorfolog-

icas de especies de un matorral mediterraneo (Andalucıa,

Espana). Acta Bot. Malacitana 23: 133–148.

Nemani R. and Running S.W. 1996. Implementation of hier-

archical global vegetation classification in ecosystem function

models. J. Veg. Sci. 7: 337–346.

Nieto Caldera J.M., Perez Latorre A.V. and Cabezudo B. 1991.

Biogeografıa y series de vegetacion de la provincia de Malaga

(Espana). Acta Bot. Malacitana 16(2): 417–436.

Noble I.R. and Gitay H. 1996. A functional classification for

predicting the dynamics of landscapes. J. Veg. Sci. 7: 329–

336.

Oberdorfer E. 1960. Pflanzensoziologische Studien in Chile. Ein

Vergleich mit Europa. Flora et Vegetatio Mundi 2.

Weinheim.

Oppenheimer H.R. 1960. Adaptation to drought: xerophytism.

UNESCO Arid Zone Research Service 15: 105–138.

Orshan G. 1982. Monocharacter growth-form types as a tool in

an analytic-synthetic study of growth forms in Mediterranean

type ecosystems. A proposal for an inter-regional program.

Ecol. Mediterranea 8: 159–171.

Orshan G. 1983. Approaches to the definition of Mediterranean

growth forms. In: Kruger F.J. (eds), et al Mediterranean

Type Ecosystems: The Role of Nutrients. Ed. Springer-Verlag,

Berlın / New York, pp. 86–100.

Orshan G., Leroux A. and Montenegro G. 1984. Distribution

of monocharacter growth form types in mediterranean plant

communities of Chile, South Africa and Israel. Bulletin de la

Societe Botanique de France (Actualites Botaniques) 131:

427–439.

Orshan G. 1986. Plant form as describing vegetation and

expressing adaptation to environment. Ann. Bot. 54: 7–37.

Orshan G. (ed.) 1989. Plant Phenomorphological Studies in

Mediterranean-type Ecosystems. Kluwer Academic Publish-

ers, Dodrecht.

Parsons D.J. 1976. Vegetation structure in the mediterranean

shrub communities of California and Chile. J. Ecol. 64: 435–

447.

Pate J.S., Dixon K.W. and Orshan G. 1984. Growth and life

form characteristics of Kwongan species. In: Pate J.S. and

Buurds J.S. (eds), Kwongan-Plant Life in the Sand Plain,

University of Western Australia, pp. 84–100.

Pereira Dıas M.H. and Barros de Sa Nogueira G. 1973. Notas

sobre Rhododendron ponticum L. subsp. baeticum (Boiss. and

Reut.) Handel-Mazzetti do Concelho de Vouzela. Bol. Soc.

Broter. 47: 125–132.

Perez Latorre A.V., Cabezudo B., Navarro T. and Nieto J.M.

1995. Caracterizacion fenologica y eco-morfologica de al-

cornocales andaluces (Malaga, Espana). Anales del Jardın

Botanico de Madrid 54: 554–560.

Perez Latorre A.V., Galan de Mera A., Deil U. and Cabezudo

B. 1996. Fitogeografıa y vegetacion del sector Aljıbico

(Cadiz-Malaga, Espana). Acta Bot. Malacitana 21: 241–267.

Perez Latorre A.V., Galan de Mera A., Navas P., Navas D., Gil

Y. and Cabezudo B. 1999. Datos sobre la flora y vegetacion

del Parque Natural de los Alcornocales (Cadiz-Malaga, Es-

pana). Acta Bot. Malacitana 24: 133–184.

Perez Latorre A.V., Galan de Mera A. and Cabezudo B. 2000.

La vegetacion caracterizada por Rhododendron ponticum L.

en Andalucıa (Espana). Una complicada historia nomencla-

tural para una realidad fitocenologica. Acta Bot. Malacitana

25: 198–205.

Perez Latorre A.V., Caritat A. and Vilar L. 2001. Use of growth

form for describing and comparing Quercus suber forest in

the Iberian Peninsula. Phytocoenologia 31(1): 109–121.

Perez Latorre A.V. and Cabezudo B. 2002. Use of monochar-

acteristic growth forms and phenological phases to describe

and differentiate plant communities in Mediterranean-type

ecosystems. Plant Ecol. 161: 231–249.

Pierce S.M. 1984. A synthesis of plant phenology in the fynbos

biome. South African National Scientific Programmes report.

Quezel P. 1985. Definition of the Mediterranean region and the

origin of its flora. In: Gomez Campo C. (ed.), Plant Con-

servation in the Mediterranean Area. Dordrecht, The

Netherlands, pp. 9–24.

Ratcliffe D.A., Birks H.J.B. and Birks H.H. 1993. The ecology

and conservation of the Killarney fern Trichomanes specio-

sumWilld. in Britain and Ireland. Biol. Conserv. 66: 231–247.

Rivas Martınez S. 1987. Memoria y Mapas de las Series de

Vegetacion de Espana. MAPA-ICONA, Madrid.

Romane F. 1987. Efficacie de la distribution des formes de

croissance pour l’analyse de la vegetation a l’echelle regio-

nale. These Docteur es science, Marseille.

Ruiz de la Torre J. 1971. Arboles y arbustos. Inst. Forestal de

Investigaciones y Experiencias, Madrid.

Sack L., Grubb P.J. and Maranon T. 2003. The functional

morphology of juvenile plants tolerant of strong summer

drought in shaded forest understories in southern Spain.

Plant Ecol. 168: 139–163.

Salvo A.E. 1990. Guıa de helechos de la Penınsula Iberica

y Baleares. Ed. Piramide, Madrid.

Smith T. and Huston M. 1989. A theory of the spatial and

temporal dynamics of plant communities. Vegetatio 83: 49–

69.

Valcarcel V. 2002. Hacia un tratamiento taxonomico de las

hiedras (Hedera L., Araliaceae) ibericas: de caracteres mor-

fologicos a moleculares. Anales del Jardın Botanico de

Madrid 59(2): 363–368.

Valdes B., Talavera S. and Galiano E.F. (eds) 1987. Flora

vascular de Andalucıa Occidental. Ed. Ketres, Barcelona.

Went F.N. 1971. Parallel evolution. Taxon 20: 197–226.

Werger M.J. and Ellenbroek G.A. 1978. Leaf size and leaf

consistence of a riverine forest formation along a climatic

gradient. Oecologia 34: 297–308.

247