Phenomorphology and Eco-Morphological Characters of Rhododendron Lauroid Forests in the Western Mediterranean (Iberian Peninsula, Spain)

Plant Ecology (2006) 187:227–247 Springer 2006 DOI 10.1007/s11258-005-6574-0 -1

Phenomorphology and eco-morphological characters of Rhododendron lauroid forests in the Western Mediterranean (Iberian Peninsula, Spain)

A.V. Pe´rez Latorre* and B. Cabezudo Departamento de Biologı´a Vegetal. Facultad de Ciencias, Universidad de Ma´laga, Apartado 59, E-29080 Ma´laga, Spain; *Author for correspondence (e-mail: [email protected]; 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 Mediterranean vegetation because of their relict nature (allegedly pre-glacial, Southern-Iberian and Pontic) and connection with 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 subtropical lauroid vegetation (greater forest stratification, larger leaves, high percentage of photosynthetic stems, scarce tomentosity, pre-flowering in a season different to Mediterranean species and closeness of autumn–winter flowering species). There are, however, links with typical Mediterranean vegetation (Quercus L. forests) that surrounds the Rhododendron stands, due to its adaptation to Mediterranean climate (sclerophyll leaves, plant and leaf duration, post-fire regeneration, fleshy fruit and fruit setting-seed dispersal seasonality). Within the community, different groups of plants show different adaptations to the same biotope, suggesting their distinct paleo-phytogeographical origins. The results confirm the singularity of this vegetation within the typically Mediterranean environment where it grows and its connections with other extra-Mediterranean types.

Introduction (Box 1996), predicting its dynamism (Noble and Gitay 1996) even detecting species outside their The use of ecomorphology (growth forms) and ecological context (Herrera 1984, 1987). In the phenomorphology to study Mediterranean vege- case of Mediterranean vegetation, the standardi- tation and flora was first proposed by Orshan sation of methodology not only allows between (1982, 1983, 1986 and 1989). Growth forms pro- ecosystems comparison but also means it can be vide information on adaptive traits (Mooney 1974; used for describing as a function of ecomorpho- Le Roux et al. 1984; Pierce 1984), while a phenological (growth forms) and phenomorphological morphological study provides data on the com- characteristics (Floret et al. 1987, 1990). The plete annual cycle concerning changes in the method has been used in Mediterranean regions of organs in relation to seasonal climatic changes and the world, including Australia (Pate et al. 1984), plant architecture. These methods, which may be Chile (Orshan et al. 1984; Montenegro et al. included in the broad definition of ‘functional 1989), France (Floret et al. 1987, 1990; Romane types’ (Box 1987), have confirmed excellent for 1987), Israel (Danin and Orshan 1990; Keshet cataloguing vegetation (Nemani and Running et al. 1990), South Africa (Le Roux et al. 1989) 1996), relating vegetation with climatic parameters and Spain (Cabezudo et al. 1992, 1993; Pe´rez 228

Latorre et al. 1995, 2001; Caritat et al. 1997; Pe´rez Latorre et al. 2000). Called ‘ojaranzal’ in Navarro and Cabezudo 1998; Castro Dıéz and Spanish, this community is uniquely found in SW Montserrat Martı´1998; Pe´rez Latorre and Cab- Iberia within western Europe (Spain and Portugal) ezudo 2002). Pe´rez Latorre and Cabezudo (2002) (Pe´rez Latorre et al. 1996) and belongs to the proposed a synthesis of the Orshan’s method to be Western Mediterranean relict lauroid vegetation applicable to Mediterranean climate regions in the (Rhododendretalia pontici Pe´rez Latorre et al. world. The synthesis was applied to woodlands 2000, Pruno-Lauretea azoricae Oberdorfer ex (Quercus suber L., Fagaceae) and shrublands (Ci- Sunding 1972) (Cabezudo and Pe´rez Latorre stus L. spp., Cistaceae) in Spain, observing clear 2001). In Spain, its most important representative distinctions between the two formations as regards is found in Andalusia (Los Alcornocales Natural both ecomorphological (growth forms) and phe- Park, Cadiz Province; Pe´rez Latorre et al. 1999) nological parameters (phenophases and related while much smaller populations are found in the indexes). Sierras de Monchique and Vouzela in Portugal Here we continue this line of work by applying (Pereira Dıás and Barros de Sa Nogueira 1973; the method proposed by Pe´rez Latorre and Cab- Malato Beliz 1982). The most unusual floristic ezudo (2002) to a type of vegetation of great paleo- characteristic of this community is the brio-pte- phytogeographical and conservation interest: the ridophytic stratum with species which have a paleomediterranean relict lauroid forests of Rho- Macaronesian-Atlantic optimum or paleomedi- dodendron ponticum L. (Ericaceae). These date terranean origin (such as Lepidopilum virens Card., from the end of the Tertiary (Que´zel 1985; Mai Tetrastichium fontanum (Mitt.) Card., Neckera 1989) and are now relegated to the extreme en- intermedia var. laevifolia (Schiffn.) Renauld and claves of western (Strait of Gibraltar) to eastern Cardot, Homalia webbiana Mont., Isopterygium (Bosphorus) Mediterranean, showing climatic bottini (Breidl.) Broth-Bryophyta-. Culcita macro- peculiarities in both sites. carpa C. Presl., Diplazium caudatum (Cav.) Jer- The main objective of this work is to characte- myPteris incompleta Cav., Vandenboschia speciosa rise and describe this kind of plant community (Willd.) Kunkel -Pteridophyta-) (Salvo 1990; Gu- using ecomorphology and phenomorphology and erra et al. 2003). to study the relationships with the ecological parameters of the biotope where it develops. An- other objective is to analyse the standardised data Study site to discuss the originality or similarity of Rhodo- dendron forest to other kind of typically Mediter- The study site was chosen taking into consideration ranean forest (Quercus suber). We also try to make the presence of most of the species belonging to the an approach to eco-phenomorphological grouping community and the state of conservation. The se- of species following a combination of their eco- lected R. ponticum stand (Figure 1) lies within a morphological and phenophasic patterns. Finally, protected area (Los Alcornocales Natural Park, we try to find characters that support the relict Los Barrios municipality, Dehesa de Ojeń) in the origin of Rhododendron forests and its eco-phe- province of Cadiz (Spain). The riparian site occu- nomorphological relations to present lauroid veg- pies a 10 m wide, 20 m long stretch at 350 m a.s.l. etation. (536¢ W/367¢ N). A permanent stream flows on siliceous sands, the bed of which contains large rocky blocks. The soil data (Table 1) point to a low Methods pH and the absence of carbonates, while climatic data (Figure 2, Table 2) reveal a typically Medi- Vegetation terranean warm climate (thermomediterranean bioclimatic belt with an average annual tempera- The studied vegetation type corresponds to ripar- ture of 17.6 C) and much rain (humid ombrotype, ian forest dominated by Rhododendron ponticum average annual rainfall of 1078 mm) although with (Scrophulario laxiflorae–Rhododendretum pontici a dry period between July and August. 229

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 Oje´n, Ca´diz province). White dots correspond to other R. ponticum forests (localities taken from (Pe´rez Latorre et al. 1999, 2000). 230

Table 1. Main soil characteristics in the area of the study site. Table 2. Weather station at Los Barrios (Polvorilla), Ca´diz (534¢ W/3615¢ N). Parameter Type/data JFMAMJJASOND Soil type Alfisol Rock type Siliceous sandstones 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 pH horizon A (H2O) 5.6 C/N horizon A 15.7 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 CO3 horizon A 0 pH horizon B (H O) 4.7 2 It (Thermicity index) = 425, lower thermomediterranean bio- C/N horizon B 11.2 climatic belt with lower humid ombrotype (Rivas Martıńez CO horizon B 0 3 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.

120 Mean annual rainfall (mm)/2 ephemerals (terophytes) and ephemeroids (some geophytes and hemicryptophytes) were not in- 100 Mean annual temperature (ºC) cluded in the studies, because their shoots disappear during the unfavourable season (Evenari 80 et al. 1975). The ecomorphological characters (growth forms) were determined for each species in 60 the field. Twenty-eight characters of those proposed by Orshan (1986) were studied as well as 40 fruit type (fleshy, dry), as proposed in (Pe´rez La- torre et al. 1995). Afterwards a species/character 20 data matrix was made and the percentage of presence of each character expression was calcu- 0 lated on the basis of number of species showing JFMAMJJASOND that character (see Appendix A). For the eco- Figure 2. Climatic diagram of the study area. morphological description of the communities and the subsequent comparison, we used the characters and indices proposed by Pe´rez Latorre and Cab- Ecomorphology ezudo (2002) including Estimated Biomass of the Species (EBS) = plant height (m) · crown diam- For this ecomorphological study, we used the eter (m) · canopy or branch density (%), and method standardised by Orshan (1982, 1986), Estimated Biomass of the Community while following the proposal by Orshan (1989) for (EBC) = sum of EBS’s of all the species. Figure 3 the phenological study. A selective plant inventory shows the relative flat form of each species and its was made in the locality, according to the presence positioning into the community structure. of the most representative species within the community. The plot measured 200 m2, enough to include the whole diversity of species. The inven- Phenology and phenophasic indices tory was made following Braun-Blanquet (1979), including environmental data and plant cover of Data concerning the different reproductive phe- the species, which was divided into persistent and nological phases (flower bud formation, flowering, non-persistent (Table 3). Following the recom- fruit setting, seed dispersal) and vegetative phe- mendations of Orshan (1986) we only took into nological phases (vegetative growth and leaf account the persistent or arid-active species (Eve- shedding of dolichoblasts and brachyblasts) were nari et al. 1975), that is to say, those that bear recorded through monthly visits during a complete aerial active shoots throughout the year and which annual cycle (2002–2003), for each arid-active or are therefore adapted to the Mediterranean persistent species (Evenari et al. 1975; Orshan drought season. Arid-passive plants such as 1989). Pteridophytes were excluded of calculations 231

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 Pe´rez Latorre et al. 1999, 2000); * = characteristic species of the community.

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 because of the lack of standard reproductive phe- Phenophasic patterns of the species were taken nophases. A minimum of 30 individuals of each from the models described by Montenegro et al. species were selected and/or marked when possi- (1989: 385) (patterns A, B, C, D, and E), although ble, while a phenomorphological herbarium a new phenophasic pattern (F) is here proposed to (MGC) with representative samples of the phe- describe the almost total coincidence of vegetative nological phases was collected. For each species a growth with those of flower bud formation and phenological calendar was drawn up (see Appen- flowering (Figure 4). dix B), excluding uncommon events (Castro Dıéz and Montserrat Martı´1998). The frequency of each phenophase taking place in each month was Nomenclature calculated for the set of species. The phenological calendar of each community was constructed as a Valde´s et al. (1987) and Castroviejo et al. (1986) function of the seasonality of the following phe- were used for this work (Valca´rcel 2002, for He- nological phases: flower bud formation, flowering, dera; Corley and Crundwell 1991, for Bryophyta). fruit setting, seed dispersal, vegetative growth and leaf shedding. The descriptions of the species and vegetation using phenophases and phenophasic Results indices (Active Phenophasic Period of the Species APS, Active Phenophasic Period of the Commu- The main ecomorphological and phenomorpho- nity APC and Index of reproductive/vegetative logical data are indicated in Appendices A and B. Activity of the Species RVA), were made following As a result, we made the ecomorphological char- the model of (Pe´rez Latorre and Cabezudo 2002). acterisation and the phenophasic calendar. 232 mseter

Quercus Quercus canariensis canariensis

15 Header Hreade slope maderensis Aslnu Frgaan ul maderensis golsutin a bicaaet

10 Liorn cae Viburnum hispanica tinus Ilex Lrausu pre ado nsobili 5 Scarophulari lalxif ora Roh dodendron Rhododernnd o Plhyail re ponticum + pmonticu + angustifolia 2.5 Ruscus Samil xe asp ra Sampil xea as r atculeusa

0 Rupscus hy ophyllum Pmtpeeris inco l ta Diplaziuaum c duat m stream

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

Ecomorphological characterisation Phenophasic calendar

Rhododendron ponticum forest: phanerophytic, For phenophasic calendar see, Figures 2, 5 and 6, scarcely spinescent, holoxyle, multi-layered and and Table 2. Flower buds formation from autumn evergreen community, with a maximum height of to spring, thus avoiding maximum temperatures 22 m. Leaves are shed periodically on average and the summer rainfall minima; peak flowering in every 18 months; the leaves are predominantly spring with a secondary maximum in autumn, sclerophyll, with a 7% degree of tomentosity, and both warm, rainy seasons with many hours of mostly of about 38 cm2 (micro-mesophyll). The daylight; peak of fruit setting in summer, coin- average duration of the plants is 34.8 years; most ciding with maximal temperatures and rainfall are adapted to after-fire regeneration by below minima, lasting into autumn with its abundant ground buds pattern. Vegetative growth and rainfall and moderate temperatures; abundant flowering mainly occur in spring and fleshy fruits seed dispersal in autumn, reaching a maximum in are predominant. winter, when temperatures are at their lowest 233

Discussion

The discussion is made following paragraphs dealing with ecomorphological characters, phenological phases, phenophasic indices, phenophasic patterns and eco-phenomorphological groups.

Ecomorphological characters

For ecomorphological characters see Tables 4 and 5.

Figure 4. Phenophasic patterns of the species that represent the Structure of the community and renewal buds phenophasic sequence and overlapping of growth and flowering. (A) first: growth, second: growth and buds overlapping, Biotype distribution (based on renewal bud posi- third: flowering. (B) first: growth, second: buds, third: flower- tion) shows that this is a forest dominated by ing, no overlapping. (C) first: growth, second: buds and growth overlapping, third: flowering and growth overlapping. (D) first phanerophytes, as occurs in other types of Medi- buds, second: flowering, third: growth, no overlapping. (E) first: terranean forests studied (Oberdorfer 1960; Ro- buds, second: flowering and growth overlapping, third: growth. mane 1987; Floret et al. 1990; Danin and Orshan (F) first: buds and growth overlapping, second: flowering and 1990; Pe´rez Latorre and Cabezudo 2002). How- growth overlapping. White rectangle = vegetative growth, grey ever, the slight difference in stratification of this rectangle = flower bud formation, black rectangle = flowering. Patterns ‘‘A’’ to ‘‘E’’ from Montenegro et al. (1989). Pat- lauroid type is quite well reflected in the scaled tern ‘‘F’’ proposed here. distribution of biotypes according to plant heights (Figure 3). The first layer of trees (‘roof’) is con- stituted by mesophanerophyte (5 species) below (though mild), the days are the shortest and rain- which there is a dense layer of microphanero- fall plentiful; dolichoblast vegetative growth phytes (3 species). Three species of vines (one maximal in spring, coinciding with an increase in phanerophyte, one amphiphyte and one chamae- temperatures, continued rainfall and moist soils; phyte) climb between these two layers. At ground dolichoblast leaf shedding maximal in summer, level and in areas of low luminosity grow crypto- coinciding with the highest temperatures and phytes (two species), hemicryptophytes (two scant, if any, rainfall, although the second peak in species) and one of the two amphiphytes, adapted winter coincides with the lowest temperatures and abundant rainfall. Vegetative Phenological Phases 100 Reproductive Phenological Phases 90 100 80 90 70 80 60 70 50 p 60 s% 40 50 p 30 s% 40 20 30 10 20 10 0 0 EFMAMJJASOND EFMAMJJASOND DVG LSD BVG LSB FBF FWL FS SD Figure 6. Time curse of the vegetative phenological phases in Figure 5. Time curse of the reproductive phenological phases in the community expressed as the monthly percentage of species the community expressed as the monthly percentage of species that show each phenophase. Dolichoblast vegetative growth that show each phenophase. Flower bud formation (FBF), (DVG), leaf shedding dolichoblast (LSD), brachyblast vegeta- flowering (F), fruit setting (FS) and seed dispersal (SD). tive growth (BVG) and leaf shedding brachyblast. 234

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.

Table 5. Comparison among communities using ecomorphological characters and phenophases. Bold characters are mean diﬀerences (data for Quercus community from Pe´rez 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 235 to the light limiting factor. The existence of this Photosynthetic organs ‘‘roof’’, which creates a favourable microclimate, is perhaps responsible for the persistence of the One of the most important aspects of the forest is rest of the substrates. Regardless of the height of the leaves area. Large leaves predominate in the the phanerophytes, canopy diameters of 2–5 m community (micro-mesophyll, 20–56 cm2), with predominate, suggesting strong competition for the presence of a very large-leafed species (Quercus horizontal space, although the height of Quercus canariensis) with 56–180 cm2 (mesophyll) and two canariensis Willd. permits it to reach diameters of ferns with megaphyll leaves. Such characteristics 15 m, while the multi-trunks growth of Rhodo- differentiate this wood even further from the dendron permits a canopy in excess of 5 m. Can- Mediterranean Q. suber forest with its predomi- opy density is generally very high (>75%), which nant leaf size of 2–20 cm2 and where it is also gradually diminishes the amount of light reaching possible to find nanophyll-leaved species successive layers, meaning that the understorey (<2 cm2). This predominance of large leaves and must be composed of shade-tolerant species, with high canopy densities provides strong shade to the large shoots and leaves, maintained by the good lower strata and the ground, almost totally humidity of the biotope (Smith and Huston 1989). inhibiting the presence of herbaceous under- The estimated biomass for this community is 27.6, growth, but preserves the relict ferns, which would placing it well above the shrublands of Cistus (0.4) otherwise disappear through the photo-destruction and even Quercus suber forests (18.3) (Pe´rez La- of its pigments (Ratcliffe et al. 1993). Only in au- torre and Cabezudo 2002). tumn and winter does the intensity of the shade diminish due to the loss of leaves of the three deciduous species (Q. canariensis, Frangula alnus Shoots, barks, post-fire regeneration ssp. baetica (Reverchon and Willk.) Rivas Goday ex Devesa and Alnus glutinosa (L.) Gaertner). The The community as a whole shows lignified shoots, biomass represented by these large leaves is only the ephemeroids (not included in the study) maintained by the favourable environmental con- are axyle (Arisarum Miller, Ranunculus L., etc.). ditions of the area with a mean temperature above Smooth barks predominate (8 species), unlike in the minimum for vegetative activity, abundant typical Mediterranean woods of Q. suber where rainfall, mists and high soil humidity levels (Wer- the predominant type is flaky (Pe´rez Latorre and ger and Ellenbroek 1978; Keshet et al. 1990), un- Cabezudo 2002). Only two species (Lonicera hi- like those found in other Mediterranean woods of spanica and Rhododendron ponticum) show shed- average humidity, such as Q. suber forests (Pe´rez ding barks (which are also flaky) leading to an Latorre and Cabezudo 2002). The predominance accumulation of this inflammable dry material on of large leaves may also be due to the low level of the floor. Two species with protective corky bark nutrients in the soil (Givinish 1987) and lent (Alnus glutinosa and Quercus canariensis) are weight by the presence of Alnus, a known nitrogen- capable of post-fire regeneration while most (12 fixer. The dense shade may explain the high per- species) regenerate by epicormic or rhizome buds centage of species with photosynthetic stems below ground level. Only ferns, the vine Lonicera (44%), three small species (Ruscus L. spp. and periclymenum subsp. . hispanica (Boiss. and Re- Scrophularia) which grows in the understorey, uter) Nyman and the amphiphyte Scrophularia Smilax aspera L., which only climbs to interme- laxiflora Lange die after fire. In this respect, Rho- diate height levels, and Hedera maderensis ssp. dodendron forests closely resemble typical Medi- iberica McAllister, whose stems remain below tree terranean Q. suber forests, although no species canopies. The most interesting case is that with aerial regenerating epicormic buds are to be regarding Ilex perado var. iberica Loes. and Laurus found (Pe´rez Latorre and Cabezudo 2002) for nobilis L., both small trees, with their long-lasting which fire would lead to temporary destruction of photosynthetic branches (3–5 years) and height of community stratification and loss for several years half a metre or more, which have low light and of low light conditions necessary for the mainte- water requirements corresponding to stress-toler- nance of relict pteridophytes and bryophytes (Salvo ant plants (long-lasting aerial parts, sclerophyll 1990; Cabezudo et al. 1995; Guerra et al. 2003). leaves, photosynthetic stems) (Grime 1979; Chapin 236 et al. 1993) but which grow in a biotope which (Danin and Orshan 1990) points to the total theoretically provides good year-round conditions. inhibition of the latter due to the conditions im- posed by the dense forest, except for the climber chamaephyte Smilax. Leaves morphology

The combination of green and glabrous leaves (15 Seasonality, fruits species), without defence against dry conditions such as hairs and resins would provide (Oppenhei- Rhododendron forest is an evergreen community, mer 1960), and horizontally inserted leaves (12 reflecting mature Mediterranean formations of species) predominates, which, together with the sucesional stages. However, there is a deciduous large areas of the leaves, produces a very attenuated contingent of three species (Alnus glutinosa, Fran- light in intermediate and low layers of the vegetation gula alnus subsp. baetica, Quercus canariensis) and produces a humid biotope (Keshet et al. 1990). which points to a certain degree of coldness and The glabrous leaves with some sclerophyll degree humidity (Keshet et al. 1990), the first of which no are in contrast with the malacophyll-glabrous longer applies, so that Alnus and Frangula, at least, combination typical of Mediterranean shrublands probably come from a floristic contingent (Euro- (Pe´rez Latorre and Cabezudo 2002). A group of Siberian), a relict of cold periglacial eras. The malacophyll-glabrous plants (Alnus and Frangula) community is characterised by plants (10 species) corresponds to winter-deciduous species whose with a predominantly spring growth pattern and leaves last less than 1 year. Sclerophyll leaf implies which include the deciduous plants, and another adaptation to water stress (Parsons 1976; Campbell six species showing multi-seasonal growth (ever- and Cowling 1985; Givinish 1987) and is therefore greens). Growth stops from mid-summer to mid- somewhat surprising in these conditions where there winter, which does not reflect the good prevailing is no lack of water (Grieve 1953). However, it is hydric and climatic characteristics (Table 2). This probably the result of the pre-Mediterranean origin disagreement reinforces the possibility of an origin of the concerned species and their relict status in differently-adapted floras. The flowering season (Axelrod 1975; Herrera 1984). Even it may reflect underlines this contradiction, since although typi- ‘ghost’ paleoclimatic conditions different from the cal Mediterranean spring flowering predominates present day (Went 1971) or simply is the result of the (6 species), two species (Alnus, Viburnum tinus L.) nutrient-poor soils (Table 1) (Mooney et al. 1983) flower in winter and two (Hedera, Smilax, climb- (with Alnus as a nitrogen-fixer) typical of tropical ers) in autumn (Herrera 1984). The species show- woods (Larcher 1977) with which R. ponticum forest ing multi-seasonal flowering or spores dispersal may be ecomorphologically related. are, curiously, relict ferns and Ruscus ssp. The Spinescence is unusual in the forest, as it is in fleshy fruits are characteristic of other Mediterra- other humid Mediterranean woods (Pe´rez Latorre nean woods (Pe´rez Latorre and Cabezudo 2002) and Cabezudo 2002) and, curiously, only appears and point to the summer availability of ground on leaves or phylloclades (Smilax, not always, Ilex, water, which disagrees with the typical and almost not always, and Ruscus spp.) and not on stems. total absence of summer rains. Long-lasting (2 or 3 years) leaves predominate, a characteristic positively associated with increased Phenological phases rainfall (Keshet et al. 1990) in Mediterranean vegetation (Orshan 1982), conferring an evergreen For phenological phases see Figure 5, 6 and 7 and appearance to the community, except in the case of Table 5. the small group of winter-deciduous and malacophyll species (Alnus, Frangula, Quercus, Lonicera) whose leaves last less than a year and which Flower buds formation probably have an origin, as floristic contingent, different to the sclerophyll evergreen species This phenophase is maintained throughout the (which, nevertheless, partially lose their leaves in year, with minimum levels in summer and maxi- summer). The phanerophytes/chamaephytes index mum in September, unlike in woods of Quercus 237 suber, when the maximum occurs in February– 2003), although few individuals of the respective March. Such long periods (lasting more than populations do so at a time. 5 months) are frequent, sometimes preceding a short flowering period (Alnus, Rhododendron, Viburnum) and sometimes lasting the whole year Seed dispersal (Ruscus); while in the case of Laurus nobilis it is due to two flowerings, one in spring and one in Dispersion shows two maxima, in autumn and autumn. The shortest period (1 month) occurs in winter, with a minimum as spring turns to sum- Quercus canariensis. mer, at which time other antagonist phenophase (flowering) is at its height, as occurs in Mediter- ranean woods of Quercus suber (Pe´rez Latorre and Flowering Cabezudo 2002). Summer dispersing species are Scrophularia laxiflora (dry fruit/nuts) and Lonicera Maximum flowering occurs in spring, reducing to hispanica, while Ruscus spp. disperses its fruits almost zero in summer, the least favourable sea- throughout the year, although always in isolated son, and with a significant secondary peak in au- individuals. The longest seed dispersal period is tumn. Spring flowering species include Frangula that shown by Alnus, Ilex and Viburnum, which baetica, Quercus canariensis, Rhododendron ponti- maintain mature fruit on their branches for up to cum and Ilex perado. Those flowering in autumn 6 months. are Hedera maderensis and Smilax aspera, while Laurus nobilis flowers in both spring and autumn, although no fruits appear in the latter. Alnus glu- Leaf shedding tinosa and Viburnum tinus flower in winter, while both species of Ruscus flower practically the whole Leaf shedding is maximal in summer, coinciding year, except in the middle of summer. Phillyrea with the dry period and decrease in the water level latifolia L. did not flower during the study period, of the stream, which is typical of evergreen species as occurred in the study of a subhumid Mediter- suffering a facultative and partial loss of dolicho- ranean wood of Quercus suber (Pe´rez Latorre and blast leaves. A second maximum occurs at the Cabezudo 2002), perhaps due to an excess of shade beginning of winter due to the presence of decid- (Sack et al. 2003). The combination of different uous species (Frangula, Quercus, Alnus) the first flowering periods and a secondary peak in autumn continuing to shed leaves until the following are similar to those detected by Pe´rez Latorre and spring. Neither Ruscus spp. nor Smilax shed their Cabezudo (op. cit.). The pteridophytes (Diplazium, leaves (phylloclades in the former) since the Pteris) sporulated throughout the year. branches are completely renewed. Quercus canariensis does not shed all of its leaves but maintains a small percentage even at the beginning of spring, Fruit setting when the new branches are formed, behaviour similar to that recorded for Quercus faginea ssp. Fructification begins in spring and is at a height broteroi (Cout.) A. Camus in Quercus suber woods throughout the summer, with a secondary peak in (Pe´rez Latorre and Cabezudo, 2002). This may be autumn and a minimum in winter, as similar to the the result of the favourable climatic conditions of pattern of Quercus suber woods observed by Pe´rez the study area. Latorre and Cabezudo (2002). Since most are fleshy fruit, it is not surprising that fructification lasts until autumn. The longest fruiting period is that of Vegetative growth Ilex perado and Laurus nobilis (8 months) and the shortest occurs in Frangula, Smilax and Lonicera Vegetative growth is maximal during the spring (2 months, despite the fleshy nature of the fruit). and is zero in August, September and October, Both species of Ruscus bear fruit throughout the unlike in other Mediterranean woods (Pe´rez La- year, the result of several flowerings and supported torre and Cabezudo 2002) where the growth, al- by the permanent shaded conditions (Sack et al. though low, continues in these months. No species 238 continues growing throughout the year, which is Active Phenophasic Period of Community (APC) perhaps surprising, given that the climatic (see 100 90 Figure 2 and Table 2) and soil (permanent riparian 80 70 water) conditions are suitable for a year-round 60 50 p growth. However, there are partial flower buds s% 40 formation and fructification peaks, which pre- 30 20 sumably compete for the resources necessary for 10 0 growth (Castro Dıéz et al. 2003). Some species do EFMAMJ JASOND keep growing for several months (7–9 months in the case of Scrophularia, Hedera and Pteris), while Rhododendron forest Quercus suber forest Diplazium is the only species that continues to grow Figure 8. Time curse of the APC index (monthly percentage of throughout the year. The shortest growth period is species that show phenophasic activity). Comparison between that of Frangula, Quercus, Rhododendron, Ilex and Rhododendron and Quercus suber communities. Phillyrea, which all last for 2 months or less. The accumulation of dead matter on the plants (bran- mentioned reasons. (Pe´rez Latorre and Cab- ches, inflorescences, etc.) is greatest in spring (80%) ezudo 2002) also identified three groups in and least in autumn (35%) (Figure 7). Mediterranean Q. suber woods, although less heterogeneous in their case. As regards the Active Phenophasic Period of Phenophasic indices the Community (APC) (Figure 8), which indicates the percentage of active species (in the sense For phenophasic indices see Appendix B. The of APS) for each month during the year, the Active Phenophasic Period of Species (APS), community as a whole shows phenophasic activ- which indicates the number of months with ity between 60 and 100% of the year, but with a favourable conditions for reproductive activity spring maximum and winter minimum, with a and growth, points to three phenomorphologi- small burst during autumn. This pattern shows cal patterns in the community. A very hetero- that, despite the good conditions of the biotope geneous group making up the majority of as regards temperature and humidity, winter species and representative of the community slows down the biomass-forming and reproduc- shows activity practically throughout the year. tive activity. In comparison, Mediterranean These are Alnus, Hedera, Ilex, Laurus, Lonicera, woods of Quercus suber showed a slightly higher Scrophularia, Rhododendron, Ruscus, Viburnum activity in winter, summer and autumn than and the pteridophytes Diplazium and Pteris. Rhododendron forest although both winter and Another group shows activity during 8– summer conditions are worse than in our study 9 months (Quercus, Smilax), while Frangula al- area. The community under study only showed a nus concentrates its activity into 4 months. Of slightly higher APS in spring. However, the special interest is Phillyrea, in whose adult overall curve obtained for the APS is almost population no reproductive phenophasic activity identical for both the Rhododendron forest and was detected, probably because of the above- Quercus suber wood. The Index of reproductive/vegetative Activity of Dead Matter the Species (RVA) (Table 6) gives an idea of the 100 90 different strategies with respect to the time and 80 DM resources spent in a balance between reproductive 70 60 and vegetative phenological phases. Most of the % 50 p

s plants (12 species), including all the trees and 40 30 shrubs, are above 1, indicating the predominance 20 of reproductive over vegetative phenophases. The 10 0 maximum was obtained by Rhododendron with 6 EFMAMJ JASOND and Ilex with 5.5. Four species (all climbers) score Figure 7. Time curse of the presence of dead matter on the less than 1, the minimum (0.33) belonging to plants shoots. the amphiphyte of the understorey Scrophularia 239

Table 6. RVA index and phenophasic patterns of the species of and F was higher in the Q. suber wood. Pattern C the community. is much less common in the Rhododendron forest. Species RVA Phenophasic patterns

Scrophularia laxiflora 0,33 C Lonicera peryclimenum hispanica 0,5 B Eco-phenomorphological groups Smilax aspera altissima 0,8 B Hedera maderensis iberica 0,86 B It is possible to create a series of eco-phenomor- Frangula alnus baetica 2F phological groups in communities by combining the Ruscus hypophyllum 2E phenophasic behaviour of the species and given eco- Viburnum tinus 2,2 E Ruscus aculeatus 2,4 E morphological characters. In this way, groups with Alnus glutinosa 3E different adaptations and behaviour can be identi- Laurus nobilis 4E fied in the same biotope and within the same com- Quercus canariensis 4F munity (Pe´rez Latorre and Cabezudo 2002). Seven Ilex perado iberica 5,5 E such groups appear in the Rhododendron forest (see Rhododendron ponticum 6D Phyllirea latifolia –D Table 7) as a function of the main flowering/spores dispersal season, phenophasic pattern and biological type (plant size) plus seasonality and leaf consistency. The result is somewhat surprising since the response of the vegetation to such a homogeneous laxiflora, which shows a predominance of vegeta- biotope with so few species shows very different tive over reproductive phenophases. Similar pat- phenophasic and ecomorphological adaptations, terns were obtained by (Pe´rez Latorre and which might suggest different contingents of plants Cabezudo 2002) in Quercus suber woods, where all adapted to the biotope over a long period of time the trees and shrubs scored above 1, except some (Herrera 1984). The only strictly winter-flowering shrubs (Cytisus L., Genista L.) and Erica arborea L. species are Alnus and Viburnum, which show a very similar phenophasic calendar and identical pattern, but very different biological types and leaves. The spring-flowering species, Frangula and Quercus, Phenophasic patterns show almost identical calendar and pattern, differ- entiating themselves from the following group in The species of the community can be grouped as follows (see Figures 4 and 9): no species have pattern A; pattern B is showed by the three climbers of the community (Hedera, Lonicera and Phenophasic patterns Smilax); pattern C (flower buds formation and 45 flowering coinciding) corresponds to the only 40 amphiphyte (Scrophularia); pattern D (Phillyrea 35 and Rhododendron); pattern E, major species (Al- 30

nus, Ilex, Laurus, Ruscus spp. and Viburnum); s 25 e i pattern F is for deciduous trees (Frangula and c 20 e

Quercus). Grouping these patterns into two basic p s% 15 types, the species can be divided into: (a) the five 10 species that grow first and then flower 5 (A + B + D) and (b) those that grow and flower 0 at the same time (C + E + F) (9 species). Similar ABCDEF phenophasic patterns were seen in the Mediterra- nean wood of Quercus suber (Pe´rez Latorre and Rhododendron forest Quercus suber forest Cabezudo 2002). There were no significant differ- ences between the communities as regards patterns Figure 9 Percentage of species presenting each phenophasic B, D, E and F, although the first three parameters pattern (A–F). Comparison between R. ponticum forest and were slightly higher in the Rhododendron forest Quercus suber forest. 240

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 WSUAWS AWE Mesophanerophyte malacophyll deciduous tree Viburnum tinus AW WSUAWWSU E Microphanerophyte semisclerophyll evergreen tall shrub Frangula alnus baetica S S UUASAWS F Mesophanerophyte malacophyll deciduous tree Quercus canariensis S S UA AW S WFMesophanerophyte 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 ––––SS 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 SSU 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. that they are deciduous. Ilex, Laurus and Rhodo- maximum trees height, sclerophylly, leaf and plant dendron are also very similar, including their duration, after-fire vegetative regeneration and fle- eco-morphological traits (especially of the leaves), shy fruits. although the first show an E pattern and the third a Among the differential features (Table 5) are the D type. With autumnal flowering, Hedera and greater number of layers in Rhododendron forest, Smilax show almost identical calendars and phe- the greater amount of estimated biomass, the nophasic patterns but differ in their architecture and predominance of smooth over flaky barks, the ecomorphology. The only species that flower in greater leaf size (micro-mesophyll), the higher summer are Lonicera and Scrophularia, with very percentage of photosynthetic stems and less similar calendar but different patterns and biologi- marked tomentosity. Phenologically, a differenti- cal types. The two species of Ruscus are, unsur- ating character is the maximum flower buds for- prisingly, very similar, with multi-seasonal mation that is reached at the beginning of autumn reproductive phenophases. Phillyrea distances itself and which lasts throughout the year, the four from all the plants of the forest because of its lack of species (25% of the total) that flower in autumn/ a reproductive phenophase, but is included in the winter and the low prevalence of the C-type phe- group of Rhododendron because of its vegetative nophasic pattern (flower bud formation and phenophases, phenophasic pattern and biological flowering during the last stage of growth). type. Diplazium and Pteris are grouped together, as The relict status of Rhododendron forest can be is to be expected, because of the level of their attributed to several factors that contrast with the pteridophytic form and multi-seasonal spores dis- prevailing Mediterranean macroclimate, such as persal (reproduction). the good conditions that prevail in riparian bio- topes throughout the year. Stress tolerance char- Conclusions acteristics, such as sclerophylly, are to be found, which may have three possible explanations: (a) the Similarities between Rhododendron forests and poor quality and low pH of the soils, (b) adaptation Quercus suber woods are phenologically reflected to water stress and (c) the possibility that the (Table 5) in fruit setting, seed dispersal, APS and community originated from an ancient subtropical phenophasic patterns. As regards common eco- vegetation during the Tertiary. The phenology morphological traits, the most important aspects follows seasonal Mediterranean rhythms and does are the almost complete absence of spinescence, not reflect the good conditions which last 241 throughout the year, since, given these, vegetative and those of Bulgaria (Strandzja) may clarify the and flowering activity might be expected through- common origin of this kind of relic paleomediter- out the year, which is not the case (zero DVG in ranean vegetation. August, September and October; minimum APC in winter). It is possible that this discordance between Acknowledgements adaptation and biotope conditions is due to an adaptation to longer cycles (several years) of Project REN 2000-1155 GLO (C.A.I.C.Y.T., drought, during which the stream would dry up Spain) ‘‘Diversidad vegetal, ecologıá y estructura completely, creating conditions similar to those de los bosques lauroides relıćticos del sur de la that would arise from the absence of rainfall. Penıńsula Ibe´rica: fitocenosis, especies crı´ticas, Lastly, the combination of evergreen-sclerophyll variabilidad gene´tica de poblaciones y conserva- leaves, average to large seeds, zoochory dispersion cioń’’ has supported the studies. Dr. J. Carrioń (fleshy fruit) and late sucesional stages points to a from the University of Murcia (Spain) and anon- flora derived from tertiary-type paleotropical con- ymous referees have made some valuable sugges- ditions (Herrera 1982, 1984; Axelrod 1975). tions on the manuscript. The paleotropical relict origin of this community may be supported by the discordance between the adaptive significance of the characters studied and the biotope where they occur, con- Appendix A. stituting a good criterion (besides floristic singularity in the bryo-pteridophytic stratum) for ecosystem conservation under EEC Directive 92/ Appendix A. 43 referring to EU ‘‘habitats’’ and as Special Plants % of Conservation Area of the future European Nat- plants ure Network 2000. Renewal bud: 531 In the Pontic area (eastern Mediterranean) mesophanerophyte Rhododendron occurs as understorey of temperate Renewal bud: 319 deciduous forests of Fagus orientalis (Filibeck microphanerophyte et al. 2004) while in the Iberian Peninsula Rhodo- Renewal bud: 16 dendron grows in Mediterranean relict lauroid escandent phanerophyte forests as this work points out. This is a thought- Renewal bud: 213 provoking point for future investigations, but we hemicryptophyte will not get out of the impasse until we gain pal- Renewal bud: 213 aeobotanical information, almost completely amphiphyte lacking at the present day. Renewal bud: 213 cryptophyte Other paths for further investigation may be Renewal bud: 16 proposed such as the eco-physiology of relic ferns chamaephyte linked exclusively to the extreme ambient of shade Organs shed: 11 69 and phenological calendar of this kind of forest. leaves Studies on functional and taxonomical relation- Organs shed: 213 amphiphyte ships of the mediterranean species of the genera Organs shed: 213 Frangula, Ilex and Laurus to their Macaronesian shoots related species will add information about the Organs shed: 16 origin of this Rhododendron forests. Remains a branches basipetal palaeobotanical mystery, up to date, the absence Plant height: 319 50–100 cm of R. ponticum in the north of Morocco, few Plant height: 319 kilometres far from the Spanish Rhododendron senseless forests. Effects of climate change in this fragile Plant height: 5–10 m 3 19 water-dependant ecosystems is other avenue of Plant height: 1–2 m 2 13 future research. Finally, phytosociological com- Plant height: 2–5 m 2 13 Plant height: 10–20 m 2 13 parisons between the Rhododendron Iberian forests 242

Appendix A. Continued. Appendix A. Continued.

Plants % of Plants % of plants plants Plant height: 20–30 m 1 6 Leaf angle mainly horizontal 12 75 Crown diameter: 2–5 m 6 38 Leaf angle mainly vertical 2 13 Crown diameter: 1–2 m 3 19 Leaf angle all transitions 2 13 Crown diameter: senseless 3 19 Leaf tomentosity: non tomentose 15 94 Crown diameter: 50–100 cm 1 6 Leaf tomentosity lower side 1 6 Crown diameter: 25–50 cm 1 6 Leaf consistency: semi–sclerophyll 7 44 Crown diameter: 5–10 m 1 6 Leaf consistency malacophyll 5 31 Crown diameter: >10 m 1 6 Leaf consistency sclerophyll 4 25 Canopy density: 75–90% 5 31 Surface resins absent 16 100 Canopy density: >90 % 4 25 Ratio leaves/assimilating stems: all assim. 956 Canopy density: 50–75% 4 25 leaves Canopy density: 25–50% 3 19 Ratio leaves/assimilating stems: leaves > 638 Stem consistency: holoxyle 15 94 stems Stem consistency: hemixyle 1 6 Ratio leaves/assimilating stems: leaves 16 Bark consistency: smooth 7 44 aprox. = stems Bark consistency: none 4 25 Life duration of plant 2–5 years 2 13 Bark consistency: flaky 2 13 Life duration of plant 5–25 years 5 31 Bark consistency: corky 2 13 Life duration of plant 25–50 years 6 38 Bark consistency: papery 1 6 Life duration of plant 50–100 years 2 13 Bark thickness <2 14 88 Life duration of plant >100 years 1 6 Bark thickness 10–20 mm 1 6 Life duration larger leaves 14–26 months 7 44 Bark thickness 20–50 cm 1 6 Life duration larger leaves 6–14 months 4 25 Bark shedding rhythm none 14 88 Life duration larger leaves <6 months 2 13 Bark shedding rhythm 2–5 years 1 6 Life duration larger leaves 26–38 months 3 19 Bark shedding rhythm >5 years 1 6 Life duration smaller leaves: no sm. leaves 15 94 Spinescence absent 13 81 Life duration smaller leaves: <6 months 1 6 Spinescence leaves 2 13 Life duration assimilating stems: no ass. stems 9 56 Spinescence stems 1 6 Life duration assimilating stems 1–2 years 2 13 Size larger leaves 20–56 cm2 10 63 Life duration assimilating stems 2–3 years 2 13 Size larger leaves >1640 cm2 213 Life duration assimilating stems 3–5 years 3 19 Size larger leaves 12–20 cm2 213 Seasonality of assimilating organs evergreen 12 75 Size larger leaves 56–180 cm2 16 Seasonality of assimilating organs winter 319 Size larger leaves 2–12 cm2 16 deciduous Size smaller leaves: no leaves 15 94 Seasonality of assimilating organs summer 16 Size smaller leaves <0.2–2 cm2 16 deciduous Length of larger leaves 5–10 10 63 Main season of shoot growth spring 10 63 Length of larger leaves >50 cm 2 13 Main season of shoot growth bi-multisea- 638 Length of larger leaves 2–5 2 13 sonal Length of larger leaves 10–20 2 13 Main flowering season spring 6 38 Length of smaller leaves: no sm. leaves 15 94 Main flowering season bi-multiseasonal 4 25 Length of smaller leaves 2–5 1 6 Main flowering season autumn 2 13 Length of photosynthetic stems: 956 Main flowering season winter 2 13 no phot. stems Main flowering season summer 1 6 Length of photosynthetic stems 531 Main flowering season: no flowering 1 6 >50 cm Vegetative regeneration after fire plant killed 4 25 Length of photosynthetic stems 20–50 2 13 Vegetative regeneration after fire below 850 Width of larger leaves 20–50 11 69 ground buds Width of larger leaves: >50 cm 5 31 Vegetative regeneration below ground non 425 Width of smaller leaves: no sm. leaves 15 94 epicormic buds Width of smaller leaves 5–10 mm 1 6 Trophic types autotrophic only 15 94 Width of photosynthetic stems: no phot. stems 9 56 Trophic types N fixing 1 6 Width of photosynthetic stems 2–3 mm 4 25 Fruit type: fleshy or fleshy cotyledons 11 69 Width of photosynthetic stems 3–5 mm 2 13 Fruit type: dry 3 19 Width of photosynthetic stems 5–10 1 6 Fruit type: no fruits 2 13 Leaf colour: all green 15 94 Leaf colour green and glaucous 1 6 243

Appendix B. 244

Appendix B. Continued. 245

Appendix B. Continued. 246

References Filibeck G., Arrigoni P.V. and Blasi C. 2004. Some phytogeographical remarks on the forest vegetation of Colchis (Wes- Axelrod D.L. 1975. Evolution and biogeography of the Mad- tern Georggia). Webbia 59(1): 189–214. rean-Tethyan sclerophyll vegetation. Ann. Mo. Bot. Gard. Floret C., Galan M.J., Le Floc’h E., Orshan G. and Romane F. 62: 284–334. 1987. Growth form as a tool in characterising vegetation of Box E.O. 1987. Plant life forms and Mediterranean environ- small areas. A trial in a Mediterranean environment. Vege- ments. Ann. Bot. 45(2): 7–42. tatio 71: 3–11. Box E.O. 1996. Plant functional types and climate at the global Floret C., Galan M.J., Le Floc’h E., Orshan G. and Romane F. scale. J. Veg. Sci. 7: 309–320. 1990. Growth forms and phenomorphology traits along an Braun-Blanquet J. 1979. Fitosociologıá. Bases para el estudio environmental gradient: tools for studying vegetation? J. Veg. de las comunidades vegetales. Ed. Blume. Madrid. Sci. 1: 71–80. Cabezudo B., Navarro T., Pe´rez Latorre A.V., Nieto Caldera Givinish T.J. 1987. Comparative studies of leaf form: assessing J.M. and Orshan G. 1992. Estudios fenomorfolo´gicos en la the relative role of selective pressures and phylogenetic con- vegetacioń del sur de Espan˜ a. I. Cistus. Acta Bot. Malacitana straints. New Phytol. (Suppl.) 106: 131–160. 17: 229–237. Grieve B.J. 1953. The physiology of sclerophyll plants. J. Roy. Cabezudo B., Pe´rez Latorre A.V., Navarro T. and Nieto Caldera Soc. West Aust. 39: 31–45. J.M. 1993. Estudios fenomorfolo´gicos en la vegetacioń del sur Grime J.P. 1979. Plant Strategies and Vegetation Processes. de Espan˜ a. II. Alcornocales mesomediterrańeos (Montes de Wiley, Chichester. Ma´laga, Ma´laga). Acta Bot. Malacitana 18: 179–188. Guerra J., Cano M.J., Pe´rez Latorre A.V., Ros R.M. and Cabezudo B., Pe´rez Latorre A.V. and Nieto Caldera J.M. 1995. Cabezudo B. 2003. Flora brio-pteridofı´tica de los bosques Regeneracioń de un alcornocal incendiado en el sur de lauroides de Rhododendron ponticum L. del Parque Natural Espan˜ a (Istań, Ma´laga). Acta Bot. Malacitana 20: 143–151. de Los Alcornocales (Ca´diz-Ma´laga, Espan˜ a). Acta Bot. Cabezudo B. and Pe´rez Latorre A.V. 2001. Notas sobre la Malacitana 28: 19–36. vegetacioń de Andalucıá. III. Acta Botanica Malacitana 26: Herrera C. 1982. Biologıá reproductiva de plantas len˜ osas 225–228. mediterrańeas: sıńdromes tropicales lejos del tro´pico. II Jor- Campbell B.M. and Cowling R.M. 1985. Relationships between nadas de Taxonomıá Vegetal. Resu´men de conferencia, vegetation structure and the environment in the Cape, Sevilla. Southern Africa: a review. Ann. Bot. 43: 245–255. Herrera C. 1984. Patrones morfolo´gicos y funcionales en Caritat A., Pe´rez Latorre A.V. and Romo A. 1997. The dis- plantas del matorral mediterrańeo del sur de Espan˜ a. Stud. tribution of ecomorphological types as related to altitude in Oecol. 5: 7–34. the Montseny mountain range (NE Spain). A preliminary Herrera J. 1987. Flower and fruit biology in southern Spanish study. Sci. Gerunden. 23: 63–71. mediterranean shrublands. Ann. Mo. Bot. Gard. 74: 69–78. Castro Dıéz P. and Montserrat Martı´G. 1998. Phenological Keshet M.A., Danin A. and Orshan G. 1990. Distribution of pattern of fifteen Mediterranean phanaerophytes from ecomorphological types along environmental gradients in Quercus ilex communities of NE Spain. Plant Ecol. 139: 103– Israel: 1. Renewal bud location and leaf attributes. Ecol. 112. Mediterranea 16: 151–161. Castro Dıéz P., Monserrat Martı´G. and Cornelissen J.H.C. Larcher W. 1977. Ecofisiologıá Vegetal. Ed. Omega, Barcelona. 2003. Trade-offs between phenology, relative growth rate, life Le Roux A., Kyriacou X.L. and Orshan G. 1984. The pheno- form and seed mass among 22 Mediterranean woody species. morphology of selected plants in Mediterranean-type eco- Plant Ecol. 166: 117–129. systems of South Africa. Bulletin de la Socie´te´Botanique de Castroviejo S. et al (eds) 1986. Flora Iberica: Plantas Vasculares France (Actualite´s Botaniques) 131: 441–450. de la Penıńsula Ibe´rica e Islas Baleares. Vols. I-XIV. CSIC, Le Roux A., Perry P. and Kyriacou X. 1989. South Africa. In: Madrid. Orshan G. (ed.), Plant Phenomorphological Studies in Chapin F.S., Autumn K. and Pugnaire F. 1993. Evolution of Mediterranean Type Ecosystems. Kluwer Academic Pub- suites of traits in response to environmental stress. Am. Nat. lishers, Dodrecht, pp. 159–346. 142: S78–S92. Mai H.D. 1989. Development and regional differentiation of Chapin F.S., Bret-Harte M.S., Hobbie S.E. and Zong H. 1996. the European vegetation during the Tertiary. Plant Syst. Plant functional types as predictors of transient responses of Evol. 162: 79–91. arctic vegetation to global change. J. Veg. Sci. 7: 347–358. Malato Beliz J. 1982. A Serra de Monchique. Flora e Vegeta- Corley M.F.V. and Crundwell A.C. 1991. Additions and çao. Serviço Nacional de Parques, Reservas e Patrimonio amendments to the mosses of Europe and the Azores. J. Paisagı´stico. Lisboa. Bryol. 16: 337–356. Montenegro G., Avila G., Aljaro M.E., Osorio R. and Go´mez Danin A. and Orshan G. 1990. The distribution of Raunkiaer M. 1989. Chile. In: Orshan G. (ed.), in Plant Phenomor- life forms in Israel in relation to the environment. J. Veg. Sci. phological Studies in Mediterranean Type Ecosystems. Klu- 1: 41–48. wer Academic Publishers, Dodrecht, pp. 347–387. Evenari M.E., Schulze D., Kappen L., Buschbom U. and Lange Mooney H.A. 1974. Plant form as related to environment. In: O.L. 1975. Adaptive mechanisms in desert plants. In: Vern- Tu¨x en R. (ed.), Handbook of Vegetation Science IV. W. berg E.J. (ed.), Physiological Adaptation to the Environment. Junk Den Haag. American Institute of Biological Sciences, New York, pp. Mooney H.A. 1983. Plant form and function in relation to 111–129. nutrient gradients. In: Day J.A. (ed.), Mineral Nutrients in 247

Mediterranean Ecosystems. South African Nature Scientist Pe´rez Latorre A.V., Galań de Mera A., Deil U. and Cabezudo Programmes Report 71: 55–76. B. 1996. Fitogeografıá y vegetacioń del sector Aljı´bico Navarro T., Nieto Caldera J.M., Pe´rez Latorre A.V. and (Ca´diz-Ma´laga, Espan˜ a). Acta Bot. Malacitana 21: 241–267. Cabezudo B. 1994. Estudios fenomorfolo´gicos en la vegeta- Pe´rez Latorre A.V., Galań de Mera A., Navas P., Navas D., Gil cioń del sur de Espan˜ a. III. Comportamiento estacional de Y. and Cabezudo B. 1999. Datos sobre la flora y vegetacioń una comunidad de badlands. Acta Bot. Malacitana 18: 189– del Parque Natural de los Alcornocales (Ca´diz-Ma´laga, Es- 198. pan˜ a). Acta Bot. Malacitana 24: 133–184. Navarro T. and Cabezudo B. 1998. Estrategias fenomorfolo´g- Pe´rez Latorre A.V., Galań de Mera A. and Cabezudo B. 2000. icas de especies de un matorral mediterrańeo (Andalucıá, La vegetacioń caracterizada por Rhododendron ponticum L. Espan˜ a). Acta Bot. Malacitana 23: 133–148. en Andalucıá (Espan˜ a). Una complicada historia nomencla- Nemani R. and Running S.W. 1996. Implementation of hier- tural para una realidad fitocenolo´gica. Acta Bot. Malacitana archical global vegetation classification in ecosystem function 25: 198–205. models. J. Veg. Sci. 7: 337–346. Pe´rez Latorre A.V., Caritat A. and Vilar L. 2001. Use of growth Nieto Caldera J.M., Pe´rez Latorre A.V. and Cabezudo B. 1991. form for describing and comparing Quercus suber forest in Biogeografıá y series de vegetacioń de la provincia de Ma´laga the Iberian Peninsula. Phytocoenologia 31(1): 109–121. (Espan˜ a). Acta Bot. Malacitana 16(2): 417–436. Pe´rez Latorre A.V. and Cabezudo B. 2002. Use of monochar- Noble I.R. and Gitay H. 1996. A functional classification for acteristic growth forms and phenological phases to describe predicting the dynamics of landscapes. J. Veg. Sci. 7: 329– and differentiate plant communities in Mediterranean-type 336. ecosystems. Plant Ecol. 161: 231–249. Oberdorfer E. 1960. Pflanzensoziologische Studien in Chile. Ein Pierce S.M. 1984. A synthesis of plant phenology in the fynbos Vergleich mit Europa. Flora et Vegetatio Mundi 2. biome. South African National Scientific Programmes report. Weinheim. Que´zel P. 1985. Definition of the Mediterranean region and the Oppenheimer H.R. 1960. Adaptation to drought: xerophytism. origin of its flora. In: Go´mez Campo C. (ed.), Plant Con- UNESCO Arid Zone Research Service 15: 105–138. servation in the Mediterranean Area. Dordrecht, The Orshan G. 1982. Monocharacter growth-form types as a tool in Netherlands, pp. 9–24. an analytic-synthetic study of growth forms in Mediterranean Ratcliffe D.A., Birks H.J.B. and Birks H.H. 1993. The ecology type ecosystems. A proposal for an inter-regional program. and conservation of the Killarney fern Trichomanes specio- Ecol. Mediterranea 8: 159–171. sum Willd. in Britain and Ireland. Biol. Conserv. 66: 231–247. Orshan G. 1983. Approaches to the definition of Mediterranean Rivas Martıńez S. 1987. Memoria y Mapas de las Series de growth forms. In: Kruger F.J. (eds), et al Mediterranean Vegetacioń de Espan˜ a. MAPA-ICONA, Madrid. Type Ecosystems: The Role of Nutrients. Ed. Springer-Verlag, Romane F. 1987. Efficacie´de la distribution des formes de Berlıń / New York, pp. 86–100. croissance pour l’analyse de la ve´ge´tation a´l’ećhelle re´gio- Orshan G., Leroux A. and Montenegro G. 1984. Distribution nale. The´se Docteur e´s science, Marseille. of monocharacter growth form types in mediterranean plant Ruiz de la Torre J. 1971. A´rboles y arbustos. Inst. Forestal de communities of Chile, South Africa and Israel. Bulletin de la Investigaciones y Experiencias, Madrid. Socie´te´Botanique de France (Actualite´s Botaniques) 131: Sack L., Grubb P.J. and Maran˜ oń T. 2003. The functional 427–439. morphology of juvenile plants tolerant of strong summer Orshan G. 1986. Plant form as describing vegetation and drought in shaded forest understories in southern Spain. expressing adaptation to environment. Ann. Bot. 54: 7–37. Plant Ecol. 168: 139–163. Orshan G. (ed.) 1989. Plant Phenomorphological Studies in Salvo A.E. 1990. Guıá de helechos de la Penıńsula Ibe´rica Mediterranean-type Ecosystems. Kluwer Academic Publish- y Baleares. Ed. Pira´mide, Madrid. ers, Dodrecht. Smith T. and Huston M. 1989. A theory of the spatial and Parsons D.J. 1976. Vegetation structure in the mediterranean temporal dynamics of plant communities. Vegetatio 83: 49– shrub communities of California and Chile. J. Ecol. 64: 435– 69. 447. Valca´rcel V. 2002. Hacia un tratamiento taxono´mico de las Pate J.S., Dixon K.W. and Orshan G. 1984. Growth and life hiedras (Hedera L., Araliaceae) ibe´ricas: de caracteres mor- form characteristics of Kwongan species. In: Pate J.S. and folo´gicos a moleculares. Anales del Jardıń Botańico de Buurds J.S. (eds), Kwongan-Plant Life in the Sand Plain, Madrid 59(2): 363–368. University of Western Australia, pp. 84–100. Valde´s B., Talavera S. and Galiano E.F. (eds) 1987. Flora Pereira Dıás M.H. and Barros de Sa Nogueira G. 1973. Notas vascular de Andalucıá Occidental. Ed. Ketres, Barcelona. sobre Rhododendron ponticum L. subsp. baeticum (Boiss. and Went F.N. 1971. Parallel evolution. Taxon 20: 197–226. Reut.) Handel-Mazzetti do Concelho de Vouzela. Bol. Soc. Werger M.J. and Ellenbroek G.A. 1978. Leaf size and leaf Broter. 47: 125–132. consistence of a riverine forest formation along a climatic Pe´rez Latorre A.V., Cabezudo B., Navarro T. and Nieto J.M. gradient. Oecologia 34: 297–308. 1995. Caracterizacioń fenolo´gica y eco-morfolo´gica de alcornocales andaluces (Ma´laga, Espan˜ a). Anales del Jardıń Botańico de Madrid 54: 554–560.