the phytogeography of european and mediterranean heath species (ericoideae, ericaceae): a...

Journal of Biogeography (1998) 25, 165–178

The phytogeography of European and Mediterranean heathspecies (Ericoideae, Ericaceae): a quantitative analysis

F O1,2, J A1 and T M3 1 Departamento de Biologıa Vegetal y Ecologıa,Universidad de Sevilla, apartado 1095, 41080 Sevilla, Spain and 3 IRNA Sevilla, CSIC, apartado 1052, 41080 Sevilla, Spain

Abstract. The geographic ranges of heath species in in range, but the association of temperate heaths with apreference for acid soils, of Mediterranean heaths withEurope and the Mediterranean and their relationships withpubescence, and of Atlantic heaths with plant height is ofenvironmental (climatic and ecogeographic) variables andinterest. Heath species richness throughout Europe and thebiological features are analysed by means of multivariateMediterranean is analysed by multiple regression analysesmethods. In particular, classifications into floristicand, apart from a strong influence of area size, a significantelements and floristic regions, DCA floristic ordinations,effect of water conditions, temperature and proximity toCCA environment-constrained ordinations and CCAsea is detected. The area with the highest heath speciesbiology-constrained ordinations are carried out. Resultsrichness is Western Mediterranean. Additional classification,of the analyses show a correspondence with conventionalordination and multiple regression analyses of heaths in theregionalization analyses based on broader criteria, and lessIberian Peninsula (Spain and Portugal, the areas with thecorrespondence with numerical analyses of other taxonomichighest heath diversity) revealed similar patterns to thosegroups at a similar scale. This lack of fit depends on thefound in Europe and the Mediterranean. The effect ofparticular history and ecology of the taxonomic groupsheterogeneity of the studied units at this latter scale isunder study. A number of climatic (temperature and waterremoved in the Iberian analysis because of the relativestress) and geographic (coast length) variables are associatedhomogeneity of the units considered at this scale.with different types of heaths according to their geographical

ranges (continental, Mediterranean, Atlantic). Biological Key words. CCA analysis, ecogeography, Erica, IberianPeninsula, Mediterranean, species richness.features of heaths account for a small part of the variation

Resumen. Se estudia la distribucion geografica de las la asociacion de los brezos templados con los suelos acidos,de los brezos mediterraneos con la pubescencia y de los brezosespecies de brezos en Europa y el Mediterraneo y sus relacionesatlanticos con el tamano de la planta. La riqueza de especiescon un conjunto de factores ambientales (climaticos yde brezos en Europa y el Mediterraneo se analiza por medioecogeograficos) y rasgos biologicos por medio de metodosde regresion multiple y, aparte de un influencia fuerte delmultivariantes. En particular, se llevan a cabo clasificacionestamano del area, se detecta un efecto significativo de las en elementos y regiones florısticas, ordenacionescondiciones hıdricas, la temperatura y la proximidad al mar.florısticas (DCA) y ordenaciones restringidas por lasEl area con mayor riqueza de especies de brezos es el oestecaracterısticas ambientales y los rasgos biologicos (CCA). Losdel Mediterraneo. Analisis adicionales de clasificacion,resultados de estos analisis muestran una correspondencia altaordenacion y regresion multiple de los brezos de la Penınsulacon la regionalizacion convencional basada en varios criteriosIberica (Espana y Portugal, las areas con mayor diversidady una menor correspondencia con los analisis numericos dede brezos) revelan patrones similares a los observados enotros grupos taxonomicos en un ambito geografico similar.Europa y el Mediterraneo. El efecto de la heterogeneidad deEsta falta de correspondencia depende de la historia y ecologıalas unidades de area a esta ultima escala es eliminado en elparticulares de los grupos taxonomicos estudiados. Variasanalisis iberico dada la relativa homogeneidad de las unidadesvariables climaticas (temperatura y estres hıdrico) y geograficasde este.(longitud de costa) estan asociadas a tipos diferentes de brezos

segun su distribucion geografica (continental, mediterranea,atlantica). Los rasgos biologicos de los brezos explican una Palabras clave. Analisis CCA, ecogeografıa, Erica,

Mediterraneo, Penınsula Iberica, riqueza de especies.parte pequena de la variacion geografica, pero debe resaltarse

Correspondence: Dr J. Arroyo, Departamento de Biologıa Vegetal yEcologıa, Universidad de Sevilla, Apartado 1095, 41080 Sevilla, Spain.

2 Present address: Institute for Plant Conservation, Botany Department,University of Cape Town, Rondebosch 7700, South Africa.

1998 Blackwell Science Ltd 165

166 Fernando Ojeda, Juan Arroyo and Teodoro Maranon

significance, since they are characteristic of many EuropeanINTRODUCTION

ericoid heathlands. Other woody species, such as gorsesIn plant geography studies, data have been presented largely (Genisteae in the Leguminosae) are also frequent in thesein a subjective way and inductive explanations have been heathlands although, as a group, they are not restricted toproposed. The achievements of this procedure, especially at these communities (Rivas-Martınez, 1979). Although theworldwide scale and when data refer to complete floras, whole Ericoideae accounts for most characteristic speciescannot be denied. The work of Takhtajan (1986) is the best of ericoid heathlands, Empetraceae and Cassiope (subfamilyand most useful example offered, although it ‘marks the Vaccinioideae in the Ericaceae) are also worth noting, butend of the old era’ in the words of Webster (1987). Ad hoc they are not included in this study because of their dif-explanations are still widespread and difficult to avoid in ferent phylogenetic lineages (Kron & Chasse, 1993). Theanalysing and interpreting biogeographic data (Hengeveld, Ericoideae subfamily (heaths thereafter) is represented in1990), and cladistic biogeography is obviously strongly Europe and the Mediterranean Basin by three genera anddependent on robust phylogenies of the taxonomic groups twenty species, although most of its taxonomic diversityunder study (Humphries & Parenti, 1986; Humphries et al., (up to 21 genera and c. 800 species) is found in a disjunct1988). On the other hand, biogeography of species groups range: East and mostly South Africa (Good, 1974; Oliver,can be analysed on the basis of their present ecological 1991).status, as a complementary approach to the influence of The biogeographic patterns of Euro-Mediterranean heaththeir history and phylogenetic relationships. Most problems species have not been studied in a comprehensive manner.inherent to subjective data presentation and analysis can be The ecology of heathlands of northern and western Europeresolved with appropriate, currently available numerical has received much attention (see reviews in Gimingham,methods. Therefore, the main limitations in the analysis 1972; Specht, 1979; Webb, 1986; Aerts & Heil, 1993;of biogeographic relationships and ecological correlations Thompson, Hester & Usher, 1995), whereas southernconcern the accuracy of biogeographic data, i.e. identity European, Mediterranean heathlands are less known.and presence of taxa in a given area, and the completeness However, these Mediterranean heathlands, althoughof species lists for this area. comparatively small in area, show contrasting patterns of

The flora of Europe is sufficiently well known and has been ecological, taxonomic and chorological diversity (Ojeda,used as a data-source for numerical methods in analytical Arroyo & Maranon, 1995; Ojeda, Maranon & Arroyo,biogeography (see Birks, 1976; Myklestad, 1993; Myklestad 1996). The importance of heaths in Mediterranean plant& Birks, 1993, for examples of several taxonomic groups). communities has been implicitly recognized in phyto-However, a potential problem is the very artificial southern sociological literature (e.g. Rivas-Martınez, 1979), but noborder of the Mediterranean Basin, that is, the exclusion

detailed quantitative study of the ecological correlates ofof northern Africa. The flora of Europe includes only the

species range (most of the species being present in thenorthern shore of the Basin, despite the Mediterranean long

Mediterranean) has been attempted.being recognized and accepted as a floristic region (seeSpecifically, three main aims are addressed in this paper:Takhtajan, 1986:119, for a list of references) and despite the

First, to detect and quantify the geographic pattern offact that there are numerous detailed studies on the limitsspecies diversity within the Euro-Mediterranean heaths,and sectors of the Mediterranean Basin (e.g. Quezel, 1978,as defined above. Secondly, to establish the relationships1985, and references therein). Hence, the sharpest floristicbetween species distribution and environmental gradientslimit in the area falls further to the south, between thedefined by several ecogeographic variables. Thirdly, toHolarctic (including the Boreal and Mediterranean regionsquantify the relationship between range of species andin the area under study) and the Palaeotropics (Takhtajan,their biological features and habitat preferences; that is,1986), and for many European plant taxa it is preferablewe hypothesize that there is some relationship betweento consider an overall analysis of the geographic range ofmorphological and ecological syndromes and geo-Europe and the Mediterranean Basin (see Bolognini &graphical distribution. We carry out an additional andNimis, 1993 for a numerical example).parallel analysis of heaths in the Iberian peninsula, whereHeaths represent a narrow group of species in the northernmost species occur and recent data are quite homogeneoushemisphere, where they are approximately restricted toin both taxonomic and geographic context. ThisEurope and the Mediterranean (de Benito, 1948; Hulten &complementary analysis also serves as a test for theFries, 1986). The meaning of ‘heath’ is somewhat loosepossible effects of heterogeneity of the units chosen in theand depends on the context, whether ecological (any plantstudy of Euro-Mediterranean heaths.species typical to heathlands) or taxonomic (species included

The ultimate purpose of this study is to detect relativelyin the subfamily Ericoideae within the Ericaceae). In thisunbiased distributional patterns and their ecologicalstudy we opt for a taxonomic definition of heaths, whichcorrelates for an ecologically meaningful and importantform a distinct species group, supported by the monophylyspecies group, and then compare these patterns with (1)of Ericoideae based on molecular phylogenies of Ericaceaeprevious subjective regionalizations based on broader,and the related Epacridaceae and Empetraceae (Kron &intuitive criteria, and with (2) results obtained by similarChase, 1993). This will minimize the distorting effect ofnumerical techniques with other species groups, in order todifferent historical events associated to species groups withascertain if some ecologically important species allow for adisparate phylogenies. Additionally, all Ericoideae species

have more or less ericoid leaves and have a distinct ecological similar regionalization.

Blackwell Science Ltd 1998, Journal of Biogeography, 25, 165–178

Quantitative phytogeography of heaths 167

METHODS scale analysis the sizes of area units studied are relativelyhomogeneous (mean of 10,264 km2, CV=45%) and theresults obtained may verify the patterns found at broaderData collectionscale (Euro-Mediterranean), where area units are moreheterogeneous in size (mean of 328,336 km2, CV=159%).The geographic area considered for this study is Europe (as

in Tutin et al., 1964–80) and the Mediterranean Basin (asin Greuter, Burdet & Long, 1984–89). In order to record

Data analysischorological information of heath species the area wasdivided into forty-seven geographic units (Fig. 2)—those Data included in the matrices were subjected to classification

and ordination techniques in order to depict and quantifyconsidered in Tutin et al. (1964–80) and in Greuter et al.(1984–89), with the exception of Azores islands. relationships between species, areas and ecogeographic and

biological variables.Data recorded for these geographic units were bothfloristic and ecogeographic. Floristic data consisted of We applied reciprocal classification of species and

geographic units by subjecting Euro-Mediterranean andpresence or absence of heath species in each unit, accordingto chorological information contained in Tutin et al. (1972) Iberian floristic matrices to respective analyses

(Hill, 1979) in order to delimit floristic elements and floristicand Greuter et al. (1986), whose nomenclature is followed.Erica andevalensis, absent in former data sources, was regions. Results of element and region classifications can be

expressed in a two-way table where cells represent the relativeincluded as a narrow, distinct endemic from a small areain SW Spain (Cabezudo & Rivera, 1980). Taxonomic abundance of each element in each region (Birks, 1976;

Myklestad, 1993; Myklestad & Birks, 1993). Classificationcategories below species level were not considered. Therebywe established a floristic matrix of twenty species in forty- analyses were performed using the package (Hill,

1979) and drawn as a hierarchical structure of floristicseven geographic units. For species names see Appendix 1.Ecogeographic data were included as two types of variable: elements and regions. Although hierarchical classification of

floristic areas is usually achieved by convenience, it has beenclimatic and geographic (eight and three variables,respectively, see Appendix 2). Climatic data were obtained as shown that floristic relationships are actually arranged in a

natural hierarchy (McLaughlin, 1992).mean values from several climatic diagrams (Walter & Lieth,1967) from weather stations homogeneously scattered in each The floristic matrices were also subjected to indirect

and direct gradient analyses. Indirect gradient analysis wasgeographic unit (average 6.9 diagrams per unit and onediagram each 35,000 km2). For some geographic units data performed using detrended correspondence analysis (DCA,

Hill, 1979; ter Braak, 1991). Canonical correspondencecorresponding to four climatic variables were not available(7.3% of blank cells in the ecogeographic matrix). Blanks analysis (CCA)—a technique for direct gradient analysis

(ter Braak, 1991)—was used and the variances explainedcorresponding to units in the Mediterranean and Borealregions were substituted with mean values corresponding to by the four first axes of DCA and CCA, respectively, were

compared to find if the ecogeographic variables consideredall utilized climatic diagrams for Mediterranean and Borealregions, respectively, given their contrasting climates (Walter can explain the major floristic gradients found by DCA.

Variables constraining the scores of species and units are& Lieth, 1967) and given that this division has long beenrecognized in plant geography (see above). represented by arrows, the correlations of these variables

to CCA axes being proportional to length, direction, andA third matrix included eleven biological characteristicsof heath species (reproductive, mostly related to pollination angle of arrows to axis. The relationship between

ecogeographic variables and species distribution was testedbiology, vegetative, and habitat, see Appendix 2) whichwere judged ecologically important at a broad scale and statistically by unrestricted Monte Carlo permutation tests

(ninety-nine permutations).hence possibly showing geographic variation.An additional analysis was carried out on heath species The relationship between floristic gradients and biological

characteristics of species was tested in a similar way byfound in the Iberian peninsula—the area showing the highestspecies diversity. We considered the species and geographic comparing DCA ordination of floristic matrix with CCA

ordination constrained by biological characteristics ofunits included in Castroviejo et al. (1993), where choro-logical information is given as presence or absence in Spanish species. The statistical significance of the relationship

between distribution of species and their biological featuresand Portuguese administrative provinces, and taxonomictreatment is very recent and consistent with our Euro- was also tested by unrestricted Monte Carlo permutation

(n=99) tests. All ordination analyses were performed usingMediterranean analysis. We established the correspondingfloristic (fifteen species×fifty-nine units), ecogeographic the CANOCO package (ter Braak, 1991).

The geographic pattern of heath-species richness and(fifty-nine units×ten variables), and biological (fifteenspecies×nine features) matrices. Climatic data are from an how it is associated with environmental characteristics was

explored by means of multiple regression analysis, whereaverage of fourteen and four weather stations for Spanishand Portuguese provinces, respectively. The ecogeographic the number of heath species in each geographic unit is the

dependent variable, and ecogeographic variables are thevariables and biological features were selected as similar aspossible to the Euro-Mediterranean analysis, although this independent ones. In order to avoid strong deviation from

normality, area size, length of coastline and mean annualwas constrained by information available in data sources (seeAppendix 2) and by a lack of variation for some biological and summer rainfall were log transformed, while summer

rainfall percentage was arcsin transformed. Additionally,features within Iberian heaths. In this complementary, finer



longitude and latitude were included as independent respective monospecific elements, the former restricted toSW Europe and the latter spreading to N Europe. The mostvariables, although they had not been included in ordination

analysis to avoid any geographic constraint on the samples. Atlantic element is the E. ciliaris species group.Given the strong variation in area size of geographic units,which could obscure the influence of other variables, two

Species ranges and environmental factorsseparate multiple regression analyses were carried out—withand without including area size among independent Indirect gradient analysis, based exclusively on floristic data

and DCA, gives the eigenvalues shown in Table 1. The firstvariables. Stepwise multiple regression analyses wereperformed, the model including only significant (P<0.05) two DCA axes have the highest eigenvalues and together

account for 34.0% of the variance (Table 1); hence onlyindependent variables (BMDP Statistical Software, 1994).these two are taken into account hereafter. DCA ordinationof species is shown in Fig. 3a. Axis 1 represents a gradient

RESULTSfrom eastern to western species, from the negative to thepositive extremes of the axis, respectively. Axis 2 can be

Floristic elements and regionsassociated to a gradient from Mediterranean species(negative scores) to continental climate species (positiveResults of analysis of classification of geographic

units into floristic regions and of species into floristic scores). In this species plot, elements obtained through are distinguished by different symbols and theyelements are shown in the two-way table included in Fig. 1.

The abundance of species in the elements shows a structured show apparent segregation that is consistent with

analysis.pattern with most species present in only a few floristicregions. Ecogeographic direct gradient analysis, as shown by CCA,

determines a drop in the eigenvalues and the percentagesof explained variance by axes in comparison with DCAFloristic regions

The eight floristic regions determined are mapped in Fig. axes (Table 1). Given that the drop is not strong, theecogeographic variables included in the analysis are2b, where divisions at first and second levels of

analysis are represented. These regions are named according sufficient to account for most of the floristic variation shownby DCA. The relative position of species in the CCA species-to their location because they are geographically quite

consistent. The main dichotomy in the classification ecogeography plot (Fig. 3b) is similar to that in DCA plot(Fig. 3a), in accordance with the small drop in eigenvalues.separates Mediterranean from temperate (Boreal) European

regions relatively well. The western Mediterranean region Table 2 includes interset correlations and t-values ofcanonical coefficients for all ecogeographic variables. Mostis included among temperate regions. It shows the highest

species richness and is very particular in its species ranges, of the t-values are lower than the critical minimum value2.1 usually suggested as indicating the likely importance ofmost of them being of Atlantic affinity within the region (see

analysis of Iberian heaths below). Second-level dichotomies external, predictor variables (ter Braak, 1991). CCA axis 1is negatively correlated with mean temperature, minimumseparate, on one hand, eastern Mediterranean and

Anatolic–Balkanic regions from central Mediterranean and temperature and water stress, and positively correlated withfrost risk period and (to much lesser extent) with meanLibyan–Maltese regions and, on the other hand, Britannic

and western Mediterranean from northern European and annual rainfall. CCA axis 2 is negatively correlated withAtlantic coast length (open sea) and positively correlatedCircumpolar–Continental regions (Figs 1 and 2). Only two

geographic units are outliers to their respective regions: with temperature range. Therefore variables correlated withaxis 1 indicate a gradient from the right—species in colderIceland is included within the Circumpolar–Continental

region, despite its Atlantic situation, and Romania belongs and wetter places (such as C. vulgaris, E. tetralix and E.cinerea)—to the left—those in warmer and drierto the northern European region, despite its continental

climate. Nevertheless, these outliers should not be very (Mediterranean) areas (E. multiflora, E. terminalis, E.scoparia, E. umbellata among others). On the second CCAsignificant since they contain only one and two species,

respectively, and one of these is Calluna vulgaris, the most axis, continentality as indicated by temperature range isassociated with species such as B. spiculifolia or E. herbacea,widespread heath in Europe.whereas temperate, Atlantic climate is associated with alarge group of species, E. vagans, E. cinerea and E.Floristic elements

The twenty heath species under study were classified into mackaiana being noteworthy. There is an overall statisticallysignificant effect of the ecogeographic variables on theseven floristic elements (Fig. 1). In order to avoid confusion

with floristic regions, elements are named after their most species distribution (P=0.01) as assessed by a Monte Carlopermutation test.representative species, usually the most abundant within

each element (see Fig. 1). The first dichotomy separates themost Mediterranean elements (i.e. E. manipuliflora and E.

Species ranges and biological featuresarborea elements, with four species each) from the remainingones, which show a more gradual division, from widespread CCA analysis of geographic range of species constrained

by their biological (morphological and habitat) featuresCalluna vulgaris element (three species) to the narrow rangeE. australis element (four species) endemic to the western shows a drop in the eigenvalues and the percentage of

explained variance for the two first axes (Table 1). TheMediterranean region. Erica erigena and E. tetralix form



FIG. 1. Two-way table of the results of of Euro-Mediterranean heath species distributions. The abundance of the species withinelements in the floristic regions is shown by size of dots. Relationships between species in floristic elements and between floristic regions areshown by dendrograms. Names of floristic elements are indicated by bold type among species in each element, and names of floristic regionsare indicated at the base of area dendrogram.

relationship between these biological features and species is positively correlated with imbricate leaves, and negativelycorrelated with revolute leaves, plant height, and flowerrange is in general non-significant, most of the variables

showing low t-values and low interset correlations (Table colour (see Table 3 and Fig. 3c). Apart from the clearassociation between pubescence and eastern Mediterranean3), except for the pubescence variable. The low number of

species and the low variability of variables considered may heaths, it is apparent that most Mediterranean heath species(e.g. E. scoparia, E. arborea, E. umbellata, E. terminalis)account for this rather low significance. More data on

ecologically important variables would be desirable, but tend to be tall, to have revolute leaves, and in part exertedstamens and small, light-coloured flowers. In contrast,they were not available and need to be obtained through field

studies, which is not attempted in this paper. Nevertheless it temperate species tend to have imbricate or ciliate leaves,deeply coloured flowers and are strongly associated withshould be noted that CCA axis 1 is negatively correlated with

species preference for acid and damp soils, and positively acid soils. The relative importance of these variables issupported by high statistical significance (P=0.01) of thecorrelated with pubescent and revolute leaves. CCA axis 2



FIG. 2. Map of Europe and the Mediterranean showing (a) the geographic units considered and their heath species number, and (b) first(thick line) and second (thin line) level dichotomies of classification of geographic units in floristic regions: Ia, Eastern Mediterraneanand Anatolic-Balkanic; Ib, central Mediterranean and Libyan-Maltese; IIa, northern European and Circumpolar-Continental; IIb, Britannicand western Mediterranean.

overall model as revealed by a Monte Carlo permutationtest.

TABLE 1. Eigenvalues and cumulative percentage variance ofspecies data accounted for by the first four axes of the detrendedcorrespondence analysis (DCA) of species distributions (1= Species richnessfloristic), the canonical correspondence analysis (CCA) of speciesdistributions and environmental variables (2=ecogeographic) and The number of heath species present in each geographicthe CCA of species distributions and biological variables (3= unit of the Euro-Mediterranean range is shown in Fig. 2a.biological) for the heaths of Europe and the Mediterranean. It is clear that areas in the western Mediterranean region

generally have the highest number of heath species. TheEigenvalues Cumulative variance (%)number of species is strongly and positively correlated(P<0.01) with mean temperature and some geographicAxis DCA(1) CCA(2) CCA(3) DCA(1) CCA(2) CCA(3)variables (coast length to both inner and open sea), whereas

1 0.664 0.519 0.554 21.0 16.4 17.5 other variables related to water availability (rainfall and2 0.413 0.403 0.412 34.0 29.2 30.5 water stress) show only moderate significant (P<0.05)3 0.163 0.209 0.328 39.2 35.8 40.9 correlations (Table 4). Stepwise multiple regression of4 0.094 0.114 0.231 42.2 39.4 48.2

ecogeographic variables on species number yields the



TABLE 2. Interset correlations and t-values of regressioncoefficients for eleven ecogeographic variables in Europe and theMediterranean.

Interset correlations t-values

Variable Axis 1 Axis 2 Axis 1 Axis 2

Area size −0.053 −0.117 2.40 −1.88Mean temperature −0.868 −0.206 −2.84 1.39Rainfall 0.350 0.043 −1.51 3.61Temperature range 0.104 0.639 −0.87 3.74Water stress −0.811 −0.123 −1.88 1.28Frost risk period 0.788 0.327 0.21 2.12Frost period 0.630 0.461 −0.69 0.08Mean min. temp. −0.680 −0.397 −0.26 −1.98Absolute min. temp. −0.740 −0.345 0.98 0.82Open sea 0.393 −0.532 −0.35 −2.00Inner sea −0.318 0.139 −1.29 −1.00

TABLE 3. Interset correlations and t-values of regressioncoefficients for eleven biological and habitat variables in Europeand the Mediterranean.

Interset correlations t-values

Variable Axis 1 Axis 2 Axis 1 Axis 2

Height 0.179 −0.613 1.30 −0.78Flower length −0.265 −0.109 −1.86 −1.13Flower shape −0.304 −0.084 −0.01 −1.11Flower colour −0.153 −0.417 0.75 1.66Ex. stamens 0.340 −0.226 1.07 −0.86Rev. leaves 0.490 −0.637 −0.29 0.25Imb. leaves −0.296 0.604 −0.33 0.83Cil. leaves −0.283 0.208 0.59 1.06Pubescence 0.521 0.179 3.23 1.79Acid soils −0.718 0.172 −2.06 −0.06Damp soils −0.471 −0.214 −0.83 −0.03

TABLE 4. Ecogeographic (independent) variables used in stepwisemultiple regression on heath species number (dependent variable)in Europe and the Mediterranean. Only variables with a partialcorrelation with P<0.05 are included in the equations (see text).

Variable t-value1 P1 t-value2 P2

Temperature range 0.37 NS 3.86 0.0004Frost risk period 1.74 NS 1.40 NSFrost risk 0.18 NS 0.95 NSRainfall 2.48 0.0176 2.28 0.0286Mean min. temperature 1.45 NS 1.36 NSAbsolute min. temp 0.005 NS 0.09 NSMean temperature 5.91 <0.0001 6.08 <0.0001Water stress −2.64 0.0118 −2.66 0.0113Area 4.44 <0.0001 — —Open sea 5.19 <0.0001 5.50 <0.0001Inner sea 2.77 0.0085 3.11 0.0035

FIG. 3. Gradient analyses of heath species in Europe and the Latitude3 0.33 NS 0.70 NSMediterranean. (a) Floristic DCA, (b) ecogeographic CCA and (c) Longitude3 1.45 NS −2.74 0.0027biological CCA. Scores for axis 1 have been multiplied by −1 inDCA(a) and CCA(c). Abbreviations for species names as in 1 Stepwise multiple regression including area size.Appendix 1, and for ecogeographic and biological variables as in 2 Stepwise multiple regression excluding area size.Appendix 2. Different symbols denote -defined floristic 3 Not included in gradient analyses.elements as in Fig. 1. NS: non-significant (P>0.05).



following equation, which explains 73.3% of the variance: environmental (ecogeographic) variables are included(CCA), the drop in eigenvalues and variance explained is

no. species=−24.77+5.92 log rain−0.67 ws+3.34 logproportionally stronger; thus the values are similar to Euro-

is+1.59 log a+5.34 log os+0.62 TMediterranean CCA analysis, despite the fact that thenumber of ecogeographic data points per unit is higher.Given the strong variation in size of geographic units aPerhaps the somewhat different climatic variables,further regression was carried out excluding this independentconstrained by the data sources, are relatively noisy invariable. This resulted in the inclusion of two additionalexplaining distributional patterns of Iberian heaths. In fact,independent (ecogeographic) variables, longitude and, moreit was not possible to include some of the important climaticimportantly, temperature range (Table 4), although thevariables used in the Euro-Mediterranean analysis (seepercentage of explained variance (71.8%) was similar:Appendix 2 and Methods); one of them (ws, water stress)

no. species=−29.84+6.14 log rain−0.70 ws+3.92 log was important in explaining species richness (see above).is−0.09 longitude+2.09 tr+7.09 log os+0.79 T Moreover, climatic variables exclusive to the Iberian analysis

(e.g. summer rainfall) are probably unimportant forGeographical areas with the highest heath speciespredicting species distributions, as would be expected innumbers are those with maritime climate (high rain,Mediterranean climates (such in most of the Iberianmoderate water stress and relatively higher meanpeninsula), where winter rainfall is more critical thantemperature) close to the sea. Consequently, SW Europesummer rainfall. A Monte Carlo permutation test showedand NW Africa have the highest heath diversity.that the overall model is significant (P=0.01), even thoughmost of t-values of variables are low.

Heaths of the Iberian peninsula CCA of floristic data and biological features of Iberianheath species also showed a drop in eigenvalues andA analysis of the fifteen Iberian heath speciespercentages of variance explained by the multivariate axessuggests a grouping of species into floristic elements thatcompared with values obtained through floristic DCA (Tableis relatively similar to elements in a Euro-Mediterranean5). This drop is similar to that involved in ecogeographiccontext, despite the lower number of species. A fourth-CCA; therefore the same conclusion applies as to the extentlevel dichotomy separated five elements: (1) E. arborea, E.to which biological features account for a meaningful partmultiflora and E. terminalis (Mediterranean element); (2) E.of floristic variation. Most of the t-values of regressionerigena and E. scoparia (widespread maritime element); (3)coefficients of variables with CCA axes are low except forE. cinerea and C. vulgaris (northern element); (4) E. tetralix,plant height (−2.45, axis 2), flower colour (−2.72, axis 2),E. australis and E. vagans (continental element); (5) E.acid soils (−2.74, axis 1) and, mainly, damp soils (−5.23,andevalensis, E. umbellata, E. lusitanica, E. ciliaris and E.axis 2). Despite the number of species and biologicalmackaiana (Atlantic element). Note that these elements arevariables being lower than in Euro-Mediterranean analysis,named in a different manner to avoid confusion with Euro-the geographic pattern of these biological features is similar.Mediterranean elements.Atlantic and northern species (e.g. E. cinerea, E. ciliaris, E.The first-level dichotomy of Iberian administrativeerigena, E. tetralix) are associated with damp and acidprovinces separates Mediterranean territories (I in Fig. 4b)soils, and have larger flowers, whereas Mediterranean (eastfrom Atlantic and continental territories (II in Fig. 4b), theIberian) species such as E. multiflora are taller, their leavesformer having a much reduced heath diversity. Second-levelare revolute, and their stamens are exerted.dichotomies (Fig. 4c) separate Almerıa province in SE Spain

Finally, species richness in the Iberian peninsula was(Ib), while the Atlantic region is split into a continentalinsensitive to size of the units (provinces), as initiallysubregion (IIa, with a disjunct range in the north-west) andhypothesized and revealed by stepwise multiple regressionan oceanic subregion (IIb). The third-level dichotomy—analysis of ecogeographic variables when area was includedshown only for oceanic subregion in Fig. 4d—distinguishesand excluded among the set of independent variables.the northern fringe (Cantabric, IIba) from the remainingMultiple regression explained 66.2% of the variance whenprovinces in the W and SW Iberian peninsula (IIbb). Finally,including area size and 63.0% when excluding it. Multiplewithin this latter range, the fourth-level dichotomy (Fig. 4e)regression equations were similar in both analyses (1:separates four areas: western continental (IIbba), eu-oceanicincluding area size, 2: excluding area size), and the(IIbbb), Huelva province (IIbbc, bearing the exclusiveecogeographic variables included in the model are exactlyendemic E. andevalensis), and Gibraltarian (IIbbd), whichthe same (see also Table 6):has a high heath diversity despite its southern range andno. species=Mediterranean character. Valladolid province (see Fig. 4a)11.91+2.57 log a−1.04 log is−1.26 T+1.10 tm (1)is excluded from the floristic regions because its flora doesno. species=not contain any heath species.18.53−1.23 log is−0.95 T+0.85 tm (2)Ordination analysis of these floristic data (DCA) revealed

a higher percentage of variance accounted by the two first Significant variables entered in the model were coastDCA axes (44%, Table 5) in comparison with similar analysis length to the Mediterranean Sea, mean annual temperature,at Euro-Mediterranean scale (see Table 1). This possibly and mean annual minimum temperature. Interestingly,reveals a less variable geographic pattern of species ranges summer rainfall was non significant in both analyses, asas is implicit in the available dataset, and may result, suggested also by the ordination analysis of species

distribution (Table 6).in part, from the lower species number. However, when



FIG. 4. Map of the Iberian Peninsula showing (a) the administrative provinces used as geographic units and their heath species number,and (b–e) first to fourth level dichotomies of classification of provinces into floristic regions. Third and fourth level dichotomiesare shown only for some of the regions. (b) I: Mediterranean, II: Atlantic-continental; (c) Ia: eu-Mediterranean, Ib: Almerıa province, IIa:continental, IIb: oceanic; (d) IIba: Cantabric, IIbb: W-SW Iberian; (e) IIbba: western continental, IIbbb: eu-oceanic, IIbbc: Huelva province,IIbbd: Gibraltarian.

DISCUSSIONTABLE 5. Eigenvalues and cumulative percentage variance of The use of multivariate techniques, and particularly two-species data accounted for by the first four axes of the detrended

way indicator species analysis, correspondence analysis andcorrespondence analysis (DCA) of species distributions (1=canonical correspondence analysis in biogeography, hasfloristic), the canonical correspondence analysis (CCA) of speciesbeen discussed in detail in recent papers (see Hill, 1991;distributions and environmental variables (2=ecogeographic) and

the CCA of species distributions and biological variables (3= Myklestad & Birks, 1993; Dzwonko & Kornas, 1994, andbiological) for the heaths of the Iberian peninsula. references therein). Therefore purely methodological aspects

will not be dealt with here. Instead, biogeographic,Eigenvalues Cumulative variance (%) ecological, and biological aspects of heath distribution in

the area under study will be focused on.Axis DCA(1) CCA(2) CCA(3) DCA(1) CCA(2) CCA(3)

1 0.397 0.209 0.243 31.1 16.4 19.1Euro-Mediterranean heaths2 0.162 0.145 0.203 43.8 27.8 35.0

3 0.103 0.068 0.093 51.8 33.1 42.3Regionalization (i.e. classification) of Europe and the4 0.048 0.032 0.071 55.5 35.6 47.9Mediterranean based on their heath distribution roughlyfits the traditional floristic separation between the Boreal



fits the traditional phytosociological regionalizationTABLE 6. Ecogeographic (independent) variables used in stepwiseregression analyses of heath species number (dependent variable) (Rivas-Martınez, 1987) based on much broader and intuitivein the Iberian peninsula. Only variables with partial correlation criteria. Within the Mediterranean territory, the separationwith P<0.05 are included in the equations (see text). found between central and eastern Mediterranean regions

(Fig. 2) is also well established (see Mediterranean floristicVariable t-value1 P1 t-value2 P2

provinces in Takhtajan, 1986:13) with the exception of Sicily,whose heath species assemblage is more similar to that inTemperature range 0.39 NS 0.95 NSthe E Mediterranean.Rainfall 0.70 NS 0.46 NS

Summer rainfall 0.46 NS 1.24 NS Gradient analysis of floristic variation and its eco-% summer rainfall 0.43 NS 1.15 NS geographic correlates shows a distinct pattern associatedMean max. temperature 0.76 NS 0.29 NS mostly to climatic rather than geographic variables (perhapsMean min. temperature 6.84 <0.0001 6.86 <0.0001 with the exception of coast length to open sea). In particularMean temperature −6.00 <0.0001 −5.61 <0.0001

there is a N–S gradient associated with temperature andArea 2.32 0.0240 — —humidity, and an E–W gradient of continentality expressedOpen sea 1.09 NS 0.91 NSmostly by temperature range. In the few examples analysedInner sea −4.40 <0.0001 −5.32 <0.0001in the literature, climatic gradients show a strong correlation

1 Stepwise multiple regression including area size. with species distribution at this broad geographic scale2 Stepwise multiple regression excluding area size. (Myklestad, 1993; Myklestad & Birks, 1993). AlthoughNS: non-significant (P>0.05). narrow endemism is very rare among the studied heath

species, these correlations show that most species arecharacteristic of a set of particular climatic conditions ratherthan spreading over the gradients, the exception being the(Eurosiberian for some authors, e.g. Mattick, 1964;

Takhtajan, 1969; Good, 1974) and the Mediterranean widespread Calluna vulgaris. In fact, Calluna seems to bethe most invasive heath species in a variety of climates,regions. Numerical hierarchical classification based on

particular taxonomic groups previously analysed has also being naturalized in N America, Mexico and New Zealand(Hulten & Fries, 1986). The floristic data sources used inshown this Boreal–Mediterranean separation, although it

does not occur as the first-level dichotomy (Pteridophytes: this study (i.e. standard floras) did not provide consistentinformation on edaphic variables (e.g. soil acidity, nutrientBirks, 1976; Salix: Myklestad & Birks, 1993), but these

analyses have not included the southern Mediterranean. availability, substrate type), that is, of the values for edaphicvariables where the species are present throughout theirHeath species, despite the small number of species,

reflects better the traditional limit between Boreal and ranges. Edaphic variation would, in principle, be very helpfulin explaining heath species distribution (cf. Gimingham,Mediterranean regions. These regions belong to different

subkingdoms (Boreal and Tethyan), with a quite different 1972; Specht, 1979; for temperate heathlands; Ojeda et al.,1995, 1996, for Mediterranean heathlands). This is alsohistory, within the Holarctic (Takhtajan, 1986). This fit is

probably associated with the fact that most heath species indicated by some edaphic qualitative associations amongthe set of biological features of species (see below).are quite conspicuous in the vegetation of vast parts of these

territories (see Gimingham, 1972; Webb, 1986; Thompson et When reproductive, vegetative and habitat characteristicsof heath species and their associations with speciesal., 1995, for temperate heathlands; Rivas-Martınez, 1979;

Ojeda et al., 1995, 1996, for Mediterranean heathlands), distribution were analysed, only a small part of thegeographic variation was explained. Nevertheless, there areand in turn marked differences in vegetation between these

two regions are firmly established in the literature (Walter, differences in the correlations presented by different typesof feature. Reproductive features related to floral biology1985). The main discrepancy between observed heath

distribution and conventional phytogeographical regional- in general show low correlations in comparison withvegetative or habitat characteristics. This is a somewhatization concerns the Iberian peninsula and NW Africa: their

heath species are mostly of temperate affinities despite their surprising result since Euro-Mediterranean heaths presentsome unique characteristics among families of woody plantsfloras, as a whole, are considered within the Mediterranean

region. Part of the W Mediterranean is therefore included with wide representation in scrublands (e.g. Cistaceae,Leguminosae, Labiatae). Heaths show a wide variety ofwithin the Atlantic temperate European territory (Britannic

plus W Mediterranean in the results of some reproductive strategies related to pollination biology,ranging from wind- to insect-pollination with someclassification; Figs 1 and 2). This anomalous limit of the W

Mediterranean boundary reflects the particular geographic intermediate cases, and associated flower features, such asexertion of stamens and flower size and colour. Floweringpattern of the heath species group, but a possible distorting

effect due to the heterogeneous limit and size of the phenology is also very variable among species even at localscale (see Arroyo & Herrera, 1988, for details on thesegeographic units must be considered. However, two facts

suggest a limited effect of area size and shape. First, due to reproductive characteristics). Euro-Mediterranean heathsreproduce in part the pattern shown by South Africanthe high heath diversity found in the W Mediterranean, this

boundary should not be artificially determined by the lack heaths, which present a much wider array of reproductivefeatures, in accordance with the overwhelmingly higherof species data. Secondly, a further analysis of species ranges

within the Iberian peninsula produces a similar pattern. diversity of species there (Rebelo, Siegfried & Oliver, 1985).Biological features related to vegetative or habitatSeparation between Britannic and W Mediterranean regions



characteristics of species do show more consistent specificity of this genus, mostly associated with wet, early-successional habitats, which makes it successful in northern,geographic patterns at a Euro-Mediterranean scale. Heathscold and repeatedly glaciated–deglaciated Europe, andare shorter in continental Europe than on the Atlantic coast,hence presents a higher species richness there (Myklestadwhere they also tend to have revolute leaves (mostly in the& Birks, 1993). However, an additional evolutionary factorsouth), whereas imbricate leaves are more frequent amongdeserving particular comment should be taken into account.continental species. Revolute leaves and mostly pubescentThe apparent high level of hybridization between willowtwigs are characteristic of southern, Mediterranean heaths.species suggests a possible hybrid and recent origin forAssociation to acid and damp soils (the two being inter-many species, although ascertaining the parents is oftencorrelated) presents the strongest gradient from north todifficult (Vicioso, 1951; Tutin et al., 1964–80). Stebbinssouth; in the Mediterranean these habitats are infrequent(1984, 1985) has postulated that in historically disturbedand hence the species associated to them are scarce. Thisplaces, such as those most suffering from the effect oftrend in habitat specificity of heaths has been previouslyglaciations, hybridization and polyploidy are promoted duereported (de Benito, 1948) but here is explicitly quantifiedmostly to the higher probability of contact between potentialat a species level. An intraspecific treatment of the rangeparents, and independently of colonizing ability of hybridvariation in edaphic conditions (as quantitative variables)swarms. Following a comparative approach, Stebbins (1984:would be especially desirable, as it has proved to be very10) exemplifies this hypothesis with willow species, whichillustrative in niche separation among co-occurring heathalso frequently show polyploidy. This could be applicablespecies within communities at local scale (Ojeda, 1995).to other genera such as Carex, which seem to show a similarHeath species (as taxonomically defined here) richness innorthwards gradient of species richness (Myklestad & Birks,Europe and the Mediterranean shows a pattern which is1993). On the other hand, in Ericoideae (heaths) naturalvery common in many taxonomic groups. There are morehybridization and polyploidy are rather rare (Stebbins,species towards southern and western territories. This1984), and in European heaths the few examples known arecorresponds to a concentration of species in the Wrestricted to Erica tetralix as one of the parents (Tutin etMediterranean, where a high number of taxonomic groupsal., 1964–80). Therefore, the species richness pattern foundof shrubby plants presents a centre of diversity (e.g.in heaths is similar to other taxonomic groups whoseCistaceae, Genisteae, Thymus: Quezel, 1981, 1985; Pons &evolutionary history is not directly linked to Quaternary IceQuezel, 1985). However, heath species are somewhatAges but to gradual speciation through adaptive radiation,different from other woody species in typical Mediterraneanwhich results in species richness increasing southwards.shrublands (maquis, garrigue) in their positive correlation

with rainfall and their negative correlation with water stress(see multiple regression equations above). Constancy of Iberian heathsgeographic and ecological patterns of species richness among

Analysis of heath distribution within the Iberian peninsuladifferent speciose taxonomic groups has been reported and showed similar patterns to that found at the Euro-quantified for the Cape floristic region in South Africa, Mediterranean scale. Therefore this zoom-like analysisincluding Ericaceae (all of them being ericoid), and rainfall confirmed the consistent nature of the geographic patternswas found to be the best predictor of species richness found. The Iberian peninsula is a microcontinent where both(Linder, 1991). Although it is rather surprising that our Mediterranean and Boreal (Eurosiberian) floristic andsmall species group does show such a consistent pattern of vegetation regions are present (Takhtajan, 1986; Rivas-species richness, this is probably related to the good fit Martınez, 1987), and this separation is, in part, shown by theof heath species ranges to floristic and vegetation small set of the fifteen Iberian heath species. Traditional (i.e.regionalization of Europe and the Mediterranean, which phytosociological) regionalization in regions, super-clearly presents a pattern of increased species richness provinces, provinces and sectors of the Iberian peninsulatowards the southwest for many taxonomic groups. If we (Rivas-Martınez, 1987) roughly fits our floristic regionsconsider the positive correlation found with mean obtained through classification of heath ranges,temperature, the area with the highest species diversity score although there are some differences in the hierarchies andis Atlantic SW Europe, where the only narrow endemic limits of territories. The separation between theheath in Europe (E. andevalensis) is found. Its origin is Mediterranean coast and the rest of the Iberian peninsulaunknown at present, but it shows a very narrow habitat (first-level dichotomy of ) is sharper than thespecificity (Soldevilla, Maranon & Cabrera, 1992; Aparicio, traditional stronger separation between Boreal and1995; Aparicio & Garcıa-Martın, 1996). Mediterranean regions (placed in different subkingdoms

Numerical analysis of other taxonomic groups yielded within the Holarctic; Takhtajan, 1986). However, limits ofcontrasting results of geographic patterns of species richness, the former territories (separated by the first-level dichotomy)probably because of the quite different ecology and are mostly coincident with the two Mediterranean super-evolutionary history of the groups studied: Pteridophytes provinces of Rivas-Martınez (1987) within the Iberianhave their highest diversity in central Mediterranean and peninsula, whereas limits of the Boreal territory arecentral Europe (Birks, 1976), and Salix is centred in Alpine approximately coincident with our third level dichotomy,and northern Europe (Myklestad & Birks, 1993). The despite regionalization being constrained by size and shapebiogeography of Salix species has been studied in detail of geographic units in the dataset, and despite the limits of

these territories being associated with a large set ofand the authors suggest a role of the particular ecological



environmental factors that are very variable at local scale (e.g. considered as important in the vegetation and flora oftemperate Europe, whereas Mediterranean heaths have beenMorla & Pineda, 1985; Moreno, Pineda & Rivas-Martınez,

1990, for the Eurosiberian–Mediterranean boundary). considered as important only at local scale. Although ourstudy does not deal with vegetation (i.e. ericoid heathlands),Central north Spain is placed into two disjunct ranges within

the Atlantic Iberian peninsula in our analysis, instead of and contribution of heaths to diversity in their communitiesis not studied here, there is a higher number of heath specieswithin the traditional east Iberian superprovince (cf. Rivas-

Martınez, 1987), although it is a transition zone where some occurring in western Mediterranean areas than in temperatenorthern and central Europe. This statement should beAtlantic heaths (mostly acidophilous in the biological

analysis) and Mediterranean heaths (mostly calcicolous) are qualified, since it has been shown that Mediterranean heathshave an intermediate character between temperate and truepresent and this placement is not strongly supported. Most

of the area of the western Iberian peninsula is coincident Mediterranean floras, and hence the western Mediterraneanis the area where heaths display, including the only endemicwith a set of three chorological provinces which in traditional

regionalization does not form an independent entity (Rivas- species, most of their diversity. This southward trend inspecies richness of Ericoideae is in agreement with the highMartınez, 1987). Thus, separation within this last range does

not fit province or sector division of traditional chorology, as diversity at community level found in detailed studies carriedout in Mediterranean heathlands of the Strait of Gibraltarshould be expected due to the small scale.

Alternatively to traditional phytosociological regional- region (Ojeda et al., 1995, 1996). This is also shown by theanalysis of Iberian heaths. This is worth remarking becauseization, there is an agglomerative hierarchical cluster

analysis of the complete endemic dicot flora (1251 taxa) of the area which accounts for most ericoid heath diversity inthe world is also of Mediterranean-type climate (i.e. the SWthe Iberian peninsula (Sainz Ollero & Hernandez-Bermejo,

1985) which produced a similar regionalization to the Cape region of South Africa).In this study we consider a number of ecogeographictraditional (Rivas-Martınez, 1987) and heath (this study)

analyses. It is remarkable that such a small group as fifteen variables and biological features associated with Euro-Mediterranean heath distribution. We do not intend to useheath species yields such similar results to those obtained

with a large portion of the flora for regions, superprovinces these variables and features in causative explanations, butthey may be useful as an exploratory analysis when specificand some provinces. This should reflect the wide range of

ecological conditions experienced by Iberian heaths, which variation of certain species is analysed, especially for speciesof central and western Europe suffering dramatic reductionaccount for most of the variation of Euro-Mediterranean

heaths. The main exception is high mountains, where the in range and abundance as a consequence of man-inducedenvironmental changes (Aerts & Heil, 1993; Stevenson &abundant endemic flora determines the delimitation of many

sectors and subsectors (mostly in SE Spain) which are not Birks, 1995; Thompson et al., 1995). From an evolutionaryperspective, a phylogenetic analysis of heath species wouldreflected by heaths, due to their scarcity in these habitats.

The ecogeographic account of floristic variation of the be desirable, and for the purposes of resolving the particularhistory of migration and differentiation, special attentionIberian heaths is similar to that of the Euro-Mediterranean

heaths, again despite the lower species number in that range should be paid to Erica arborea, the only living link betweenEuro-Mediterranean and sub-Saharan heaths (Quezel, 1978).and the somewhat different ecogeographic variables used.

A similar conclusion can be reached on the correspondencebetween Euro-Mediterranean and Iberian analyses of ACKNOWLEDGMENTSbiological features and floristic variation. The strong

Most of the research was funded by National Geographiccorrelation of heath range and soil specificity of heaths isSociety (4474-91) and DGICYT (PB91-0894) grants. Prof.even stronger at Iberian scale and seems to be responsibleH.J.B. Birks, A. Aparicio and two anonymous reviewersfor the clear separation between Mediterranean and Atlanticprovided helpful comments. F.J. Salgueiro helped withheaths of the Iberian peninsula (see above), the formercomputer design of map figures and J.M. Rubio advisedbeing more typical of basic, dry soils, which are morecompiling climatic data.frequent in eastern Spain (Guerra Delgado, 1966).

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Mattick, F. (1964) Ubersicht uber die Florenreiche und Stevenson, A.C. & Birks, H.J.B. (1995) Heaths and moorland: longFlorengebiete der Erde. A. Engler’s Syllabus der Pflanzenfamilien, term ecological changes, and interactions with climate and people.II Band, pp. 626–629. Gebruder Borntraeger, Berlin. Heaths and moorland: cultural lanscapes (ed. by D.B.A.

McLaughlin, S.P. (1992) Are floristic areas hierarchically arranged? Thompson, A.J. Hester and M.B. Usher), pp. 224–239. ScottishJ. Biogeogr. 19, 21–32. Natural Heritage, Edinburgh.

Moreno, J.M., Pineda, F.D. & Rivas-Martınez, S. (1990) Climate Takhtajan, A. (1969) Flowering plants—origin and dispersal. Oliverand vegetation at the Eurosiberian–Mediterranean boundary in & Boyd, Edinburgh.the Iberian Peninsula. J. Veg. Sci. 1, 233–244. Takhtajan, A. (1986) Floristic regions of the world. University of

California Press, Berkeley.Morla, C. & Pineda, F.D. (1985) The woody vegetation in the



ter Braak, C.J.F. (1991) CANOCO v. 3.12. Agricultural n(b): no. of months with frost (E)Mathematics Group, Wageningen. rain: mean annual rainfall (E, I)

Thompson, D.B.A., Hester, A.J. & Usher, M.B. (eds) (1995) Heaths sr: summer rainfall (I)and moorland: cultural landscapes. Scottish Natural Heritage, %sr: percentage of summer rainfall (I)Edinburgh. tM: mean maximum temperature of the coldest

Thompson, D.B.A., McDonald, A.J., Marsden, J.M. & Galbraith,month (I)C.A. (1995) Upland heather moorland in Great Britain: a reviewtm: mean minimum temperature of the coldestof international importance, vegetation change and somemonth (E, I)objectives for nature conservation. Biol. Conserv. 71, 163–178.ta: minimum absolute temperature of theTutin, T.G., Heywood, V.H., Burges, N.A., Moore, D.M., Valentine,

D.H., Walters, S.M. & Webb, D.A. (eds) (1964–1980) Flora coldest month (E)Europaea, vols 1–5. Cambridge University Press, Cambridge. T: Mean annual temperature (E, I)

Vicioso, C. (1951) Salicaceas de Espana. Instituto Nacional de ws: water stress (as no. of months with rain/Investigaciones y Experiencias, Madrid. T <2) (E)

Walter, H. (1985) Vegetation of the Earth and ecological systems ofGeographic variablesthe geo-biosphere, 3rd edn. Springer Verlag, Berlin.

a: area size of the geographic units (E, I)Walter, H. & Lieth, H. (1967) Klimadiagramm-Weltatlas. V.E.B.Gustav Fischer Verlag, Jena. os: coast length to open sea (E, I)

Webb, D.A. (1955) Biological flora of the British Isles: Erica is: coast length to inner sea (E, I)mackaiana Bab. J. Ecol. 43, 319–330.

Biological variables∗∗Webb, N.R. (1986) Heathlands. Collins, London.fw col: flower colour (green=0, white=1,Webster, G.L. (1987) Book review: ‘Floristic regions of the world’pink=2, purple=3; E, I)by A. Takhtajan. Ecology, 68, 2065–2066.fw len: flower length (continuous; E, I)

APPENDIX 1. List of heath species in Europe and the fw sh: flower shape (urceolate=1, non-Mediterranean. Asterisks denote species present in the urceolate=0; E)Iberian peninsula. exer: exerted stamens (yes=1, no=0; E, I)

cil: ciliate leaves (yes=1, no=0; E, I)Species Abbreviation rev: revolute leaves (yes=1, no=0; E, I)

imb: imbricate leaves (yes=1, no=0; E, I)Calluna vulgaris L. (Hull)∗ CVU pub: pubescent leaves and twigs (yes=1, no=Bruckenthalia spiculifolia (Salisb.) Reichenb. BRU 0; E)Erica andevalensis Cabezudo & Rivera∗ EAN height: plant height (continuous; E, I)Erica arborea L.∗ EAR acid: acidic soils (yes=1, no=0; E, I)Erica australis L.∗ EAU damp: damp soils (yes=1, no=0; E, I)Erica bocquetii (Pesmen) P.F. Stevens EBOErica ciliaris L.∗ ECI ∗Obtained from Walter & Lieth (1967) for Europe and theErica cinerea L.∗ ECN Mediterranean and from Lines Escardo (1970), Font TullotErica herbacea L. EHB (1983), Rivas-Martınez (1987) and Rivas-Martınez et al.Erica erigena R. Ross∗ EER (1990) for the Iberian peninsula.Erica lusitanica Rudolphi∗ ELU ∗∗Obtained from Tutin et al. (1972), Arroyo & HerreraErica mackaiana Bab.∗ EMC (1988), Castroviejo et al. (1993), Webb (1955), BannisterErica manipuliflora Salisb. EMA (1965, 1966), Davis (1978) and Pignatti (1980).Erica multiflora L.∗ EMUErica scoparia L.∗ ESCErica sicula Guss. ESIErica terminalis Salisb.∗ ETM

BIOSKETCHESErica tetralix L.∗ ETTErica umbellata L.∗ EUM The authors are members of the research group ‘Ecology,Erica vagans L.∗ EVA Evolution and Conservation of Mediterranean Plants’.

Their main aim is to study plant diversity at taxonomic,ecological, biogeographical and genetic levels (i.e.APPENDIX 2. List of ecogeographic and biologicalbiodiversity) and to search for biological correlates. Mostvariables recorded for Euro-Mediterranean (E) and Iberianof this research has been undertaken in the Strait of(I) geographic units considered and biological variablesGibraltar region (Spain and Morocco), a ‘hot spot’ ofrecorded for the heath species.plant biodiversity. Currently they are working on the

Ecogeographic variables∗ processes determining biodiversity, at population level,funded by grants from the Spanish and AndalusianClimatic variablesgovernments.tr: intra-annual temperature range (E, I)

n(a): no. of months with frost risk (E)


the phytogeography of european and mediterranean heath species (ericoideae, ericaceae): a...

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