Broad-Scale Biodiversity Pattern of the Endemic Tree Flora of the Western

ECOGRAPHY 26: 429–444, 2003

Broad-scale biodiversity pattern of the endemic tree ﬂora of the Western Ghats (India) using canonical correlation analysis of herbarium records

C. Gimaret-Carpentier, S. Dray and J.-P. Pascal

Gimaret-Carpentier, C., Dray, S. and Pascal, J.-P. 2003. Broad-scale biodiversity pattern of the endemic tree ﬂora of the Western Ghats (India) using canonical correlation analysis of herbarium records. – Ecography 26: 429–444.

A crucial step in understanding the origin and maintenance of biological diversity is the assessment of its distribution over space and time and across environmental gradients. At the regional scale, two important attributes of species can be assessed that provide insight into speciation processes: species geographical and environmental ranges. The endemic tree flora of the Western Ghats is an interesting case for analyzing broad-scale biodiversity patterns because of the steep environmental gradients that characterize this tropical region of India. We analysed species geographical and environmental ranges by Canonical Correlation Analysis of point data from herbarium collections. We performed partial analyses to discriminate spatial and environmental correlates of species distribution, and evaluate the contribution of higher taxonomic ranks to these ranges. We identified different levels of organization in the distribution of endemism: 1) general features, such as the concentration of endemic species in the southern part of the Western Ghats, and the decrease in endemic species richness along the altitudinal and the dry season length gradients, and 2) patterns specific to genera or families, such as species niche separation along the environmental gradients. Our analyses enabled us to formulate hypotheses about the diversification of the endemic tree flora of the Western Ghats. They also confirm the value of Canonical Correlation Analysis as the suitable method for collection data analysis.

C. Gimaret-Carpentier, Dept Ecology, E6olution and Marine Biology, Uni6. of Califor- nia at Santa Barbara, Santa Barbara, CA 93106, USA (present address: UMR CNRS 5558, Lab. de Biome´trie et Biologie E6oluti6e, Uni6. Lyon I, 43 bd du 11 no6embre 1918, F-69622 Villeurbanne, France.–S. Dray (correspondence: [email protected] lyon1.fr) and J.-P. Pascal, UMR CNRS 5558, Lab. de Biome´trie et Biologie E6oluti6e, Uni6. Lyon I, 43 bd du 11 no6embre 1918, F-69622 Villeurbanne, France.

Increasing awareness of the ongoing loss of biological and evolutionary factors (Ricklefs and Schluter 1993). diversity has heightened interest in its estimation, Species geographical and environmental ranges are origin, function, and maintenance (Hawksworth 1995, two important attributes of species that can be as- Heywood and Watson 1995). The assessment of biodi- sessed at such a scale and can provide insights into versity patterns over space and time and across envi- speciation processes. Indeed, allopatric and sympatric ronmental gradients is a crucial step in the modes of speciation have different effects on the geo- understanding of these issues. With the development graphical ranges of sister taxa (Taylor and Gotelli of macroecology, broad-scale biodiversity patterns 1994, Barraclough and Vogler 2000), whereas species have been recognized (Brown 1995). These approaches niche differentiation may indicate adaptive radiation have emphasized the importance of processes that act (Knox and Palmer 1995, Schluter 1996, Losos et al. at the regional scale, combining ecological, historical 1998).

ECOGRAPHY 26:4 (2003) 429 The endemic tree flora of the Western Ghats is an methods aims at modeling species communities, analyz- interesting case for investigating broad-scale biodiver- ing the spatial and environmental distribution of species sity patterns. The Western Ghats form a 1500 km-long diversity (Guisan et al. 1999). In the context of unimo- escarpment parallel to the southwestern coast of the dal species response curves, Canonical Correspondence Indian Peninsula, recognized as one of the world biodi- Analysis (CCA; ter Braak 1986) is very efficient to versity hotspots (Myers et al. 2000). The interaction of investigate niche separation along environmental gradi- the summer monsoon winds with the relief of the Ghats ents. CCA requires a table containing abundances or results in two steep environmental gradients, a west- presence-absence of species at a series of sites and east decrease in rainfall and a south-north increase in measurements of environmental variables for the same dry season length, that determine strong changes in the sites, where a site is ‘‘the basic sampling unit, separated vegetation. The western side of the Ghats supports wet in space or time from other sites’’ (ter Braak 1986, p. evergreen forests, whereas the eastern side supports 1167). In principle, CCA can be extended in the case of deciduous forests, with the exception of a belt of dry herbarium data by dividing the study area into smaller evergreen forests in the south (Pascal 1988). In the units, such as grid cells. Number of records are then north, the wet evergreen forests are displaced by decid- computed for each cell and variations in species diver- uous formations because of the lengthening of the dry sity are analyzed from these units (Hill 1991, Bolognini season. As a consequence, the evergreen forests of the and Nimis 1993, Heikkinen 1996). However, if one uses Western Ghats are isolated from their counterpart in spatial units defined a posteriori, one cannot control the north-eastern part of India, a feature that may the sampling effort, which may biase the analyses (spe- explain their high level of endemism: 63% of the ever- cies absences are more likely to result from a poor green tree species are endemic to this region (Ramesh sampling effort). Moreover, the size of the cells can and Pascal 1991). The uplift of the Western Ghats influence the results (Gaston 1994, Bo¨hning-Gaese would date from the Pliocene; the concomitant decrease 1997, Donald and Fuller 1998). In particular, the rela- in rainfall and increase in dry season length would have tionships between species occurrences and environment induced the replacement of the wet evergreen forests of will not be tightly coupled because environmental data the Indian Peninsula by deciduous forests and the are then averaged at the cell scale. formation of dry evergreen forests in the south on the In this paper, we use a general method based on eastern side of the Ghats, while reducing the area Canonical Correlation Analysis (CANCOR, Hotelling formerly occupied by wet evergreen forests to the west- 1936) to assess variations in species diversity directly ern side of the Ghats and the north-eastern region of from a list of independent species occurrences, such as Assam (Legris and Meher-Homji 1982). So the endemic geo-referenced herbarium specimens. We show that tree species of the Western Ghats share a common CANCOR, which was found ineffective for ordination biogeographic history since the isolation of the ever- of real releve´s (Gauch and Wentworth 1976), is espe- green forests, and their geographical and ecological cially suitable for collection data. Our aim was to ranges can be compared to provide insights into specia- analyze the distribution of tree endemism in the West- tion processes (Taylor and Gotelli 1994). ern Ghats; we assessed broad-scale biodiversity patterns One way to assess species distributions consists of using different kinds of analyses in order to reveal gathering available records from the collections in mu- different levels of organization. seums or herbaria (Mourelle and Ezcurra 1996, Skov and Borchsenius 1997, Shaffer et al. 1998, Parmesan et al. 1999, Peterson et al. 1999). However, as stressed by Material and methods Ponder et al. (2001), these data suffer from several Presentation of the data set biases: they can provide reliable data about species presence, but species absence is generally dubious due To depict the geographical ranges of the endemic ever- to geographical gaps in the sampling effort. Moreover, green tree species of the Western Ghats, Ramesh and each record is uniquely characterized by the identity of Pascal (1997) gathered occurrences from three sources: the collector, the place and the date of record, so it 1) specimens in herbaria, 2) published data and 3) corresponds to a distinct sampling unit which does not results of field surveys by the French Institute of provide any information about the presence of other Pondicherry and other botanists. From this database species: local species diversity cannot be assessed di- we extracted the 5142 occurrences that correspond to rectly from such data. herbarium specimens, forming a set of reliable and Two sets of methods have been developed to deal independent observations, verified by the same expert with collection data. The first set of methods aims at (a botanist from the French Institute). Taxa represented modeling individual species distribution, coupling point by B5 occurrences were not considered, as their geo- data with abiotic variables to define species habitat graphical range could not be assessed properly. A total requirements (Stockwell and Peters 1999, Bonn and of 224 endemic tree species, belonging to 104 genera Schro¨der 2001, Ponder et al. 2001). The second set of and 38 families, were documented.

430 ECOGRAPHY 26:4 (2003) The 5142 species occurrences occupy 8 degrees of A table Y describes the environmental features at each latitude, from 8° to 16°, the area covered with evergreen locality where yik represents the measurements of the forests delimited towards the east by the isohyet 2000 kth environmental variable recorded for the ith occur- mm (Fig. 1). In this region, the escarpment of the rence (Fig. 3). As noted above, species occurrences such Ghats consists almost exclusively of archean rocks with as herbarium specimens are independent observations, varying degrees of metamorphism, and the soils (satu- so they represent the actual statistical units. As a conse- rated acidic soils) appear homogeneous (Bourgeon quence, tables X and Y represent two sets of variables 1989). Studies carried out by the French Institute of measured on the same statistical units, the 5142 occur- Pondicherry (e.g. Pascal 1992, Ramesh et al. 1997) have rences. In this case, the number of observations is much shown that, at the regional scale, species turnover is higher than the number of variables. Such characteris- driven by three climatic factors: variation in total an- tics correspond exactly to the requirements of CAN- nual rainfall, rainfall seasonality (dry season length) COR, a method that finds the linear combinations of and temperature, associated with altitude. So, we as- one set of variables that are maximally correlated with sessed species environmental ranges by compiling these linear combinations of another set of variables (Gittins data for each occurrence (Fig. 2). Altitude was recorded 1985). for each specimen in the database, while mean total As X is formed by variables indicating species mem- annual rainfall and mean annual dry season length were bership, the CANCOR of X and Y finds linear combi- deduced from bioclimatic maps of the Western Ghats nations of environmental variables that best (Pascal 1982). The dry season is defined by the number discriminate the species. This is equivalent to Discrimi- of months during which the amount of rainfall mea- nant Analysis (DA) of Y by the specific groups of sured in mm is lower than twice the temperature ex- occurrences in X (Lebart et al. 1984), also known as pressed in °C (Bagnouls and Gaussen 1953). Canonical Variates Analysis (James and McCulloch 1990). DA has been used in ecology by Green (1971), and Lebreton et al. (1988) demonstrate that Green’s Canonical Correlation Analysis of species DA is mathematically equivalent to the CCA of ter occurrences Braak (1986). ter Braak and Verdonschot (1995) admit this link and specify that ‘‘the main difference between Species information concerning the 5142 occurrences CCA and discriminant analysis is that the unit of the gathered from natural history institutions is contained statistical analysis in discriminant analysis is the indi- in a species by occurrences table X with xij =1iftheith occurrence belongs to the jth species, otherwise x =0. vidual, whereas it is the site in CCA’’. Hence, just like ij CCA, our CANCOR approach provides linear combinations of environmental variables that maximize species niche separation. CANCOR of occurrence data can be viewed as a CCA without any sampling site. Con- trary to multivariate analyses based on a partition of the study area into grid cells, CANCOR computes species environmental means directly from the list of occurrences, i.e. only from species presences. Sampling bias associated with the use of cells is thus removed. The analysis allows a direct comparison of species environmental ranges, i.e. abiotic realized niches. We defined species niches by ellipses containing 50 percent of species occurrences on the canonical planes, following the procedure described by Thioulouse and Chessel (1992) and Pe´lissier et al. (2002). We analyzed species geographical ranges in a similar way, with the table Y containing now polynomial functions of the geographic coordinates of species occurrences, i.e. the variables x, y, x2, xy, y2, etc., where x and y are, respectively, occurrence longitude and latitude. The CANCOR of X and Y becomes a Canonical Correlation Trend Surface Analysis (CCTSA) (cf. Git- tins 1968, Wartenberg 1985). This analysis identifies multispecies spatial patterns, i.e. gradients of species Fig. 1. Study area and location of the 5142 herbarium speci- composition or areas of high endemism, according to mens. the degree of overlap among species ranges. In order to

ECOGRAPHY 26:4 (2003) 431 Fig. 2. Variation of the three main environmental factors in the Western Ghats. Mapping of occurrence values by contour curves computed over the 1000 nearest occurrences for a) altitude (m), b) mean annual dry season (months), c) mean annual rainfall (mm).

visualize these patterns, we computed contour curves spatial patterns and identify other correlates of species from the canonical scores mapped on the study area, distribution, such as geographical barriers to dispersal, following Thioulouse et al. (1995). and 2) to analyze the contribution of higher taxonomic levels to species geographical and environmental Partial analyses ranges. In the latter case, the partial analyses are simi- CANCOR permits partial analyses to study the rela- lar to within-group analysis, depicting species-environ- tionships between X and Y. In this case, Y contains ment relationships or multispecies spatial patterns variables from which the effect of another set of ex- within genera or within families. planatory variables has been removed. Principles of the method are the same as those used for partial CCA (ter Permutation test Braak 1988). The mathematical details are explained in The statistical signiﬁcance of the results of CANCOR Pe´lissier et al. (2002), following Me´ot et al. (1998). We can be evaluated by a random permutation test (Manly used these partial analyses in two ways: 1) to remove 1991). First, the number of eigenvalues of interest (l) is the effect of environmental factors on the multispecies determined from the graph of the decrease in CAN-

432 ECOGRAPHY 26:4 (2003) Fig. 3. Occurrences-by-species (X) and occurrences-by- environment (Y) tables obtained from a list of n occurrences distributed among s species and characterized by p environmental variables. Species appear as dummy variables indicating species identity, while the environmental factors are considered as quantitative variables.

COR eigenvalues, and the sum of the l first eigenvalues several endemic species are restricted to this region is computed; CANCOR eigenvalues are equal to the (Fig. 4b). However, the variation in endemic species square of the canonical correlation coefficients, so the composition from the southeast is not uniform, with sum of eigenvalues measures the strength of the steep gradients of b-diversity observed towards the correlation between X and Y. Then the rows of Y are coast and the tops of the Ghats, whereas the change in permuted randomly and CANCOR analysis is endemic species composition towards the north appears performed between X and the permuted table Y. We much less marked. performed 1000 permutations and computed the sum of the l first eigenvalues for each one. We compared the results obtained from the original data set with those obtained after permutations of the rows of Y to obtain Multispecies spatial patterns independent of a p-value. environmental factors All calculations and related graphs were generated with ADE-4 software (Thioulouse et al. 1997), available We performed a partial CCTSA to remove the effect of on the internet at Bhttp://pbil.univ-lyon1.fr/ADE- environmental variables and analyze the residual com- 4/\. The maps were generated with Arcview 3.2. ponent of species distribution (the same polynomial functions of geographical coordinates were used). The first two factors were highly significant, representing 52% of total variance (pB0.001). The canonical Results correlation coefficients were smaller than in the previ- Multispecies spatial patterns ous analysis, 0.483 and 0.466. They reveal more compli- cated spatial patterns, confirming the strong correlation To obtain a general picture of the distribution of between environmental factors and species distribution endemism in the Western Ghats, we first analyzed the (Fig. 5). Species canonical scores (obtained as the cen- changes in endemic species composition in the study troid of their occurrence scores) allows the identifica- area by means of CCTSA, using polynomial functions tion of species groups sharing the same spatial features; of the geographic coordinates of order less than four, the occurrences of species representing each group can i.e. the 9 variables x, y, x2, xy, y2,x3,x2y, xy2 and y3 (x then be mapped by their physical coordinates. and y are, respectively, occurrence longitude and The first axis highlights species with narrow latitudi- latitude). nal ranges (Fig. 5a). At the negative end, there are The analysis produced two highly significant factors species whose distributions are limited to the central representing 52% of total variance (pB0.001). The part of the study area between 10 and 12°N, such as canonical correlation coefficients of these first factors Pithecolobium gracile at low elevation or Euonymus were respectively 0.747 and 0.655. The first factor re- angulatus at medium elevation, whereas at the positive veals a strong change in endemic species composition end, there are two kinds of species: 1) species whose from the coast towards the top of the Ghats, and the geographical ranges are limited to the southern moun- progressive disappearance of this b-diversity gradient in tains, and more specifically occurring on their eastern the northern part of the study area (Fig. 4a). The side, such as Garcinia tra6ancorica and Diospyros foli- second factor highlights the floristic distinctness of the olosa, and 2) species restricted to the northwestern part southeastern part of the study area, revealing that of the study area, such as Mammea suriga. Three

ECOGRAPHY 26:4 (2003) 433 Fig. 4. Multispecies spatial patterns obtained by CCTSA. Mapping of occurrence canonical scores by contour curves computed over the 500 nearest neighbours. a) ﬁrst factor, b) second factor. The colours reﬂect variation in occurrence scores (cf. insert).

floristic regions are thus delineated, each of which of Palni and Nilgiri mountains, such as Microtropis harbours a specific endemic tree flora (Fig. 5a). microcarpa and Rhododendron nilagiricum. An overlap The second axis highlights species with narrow longi- of species geographical ranges is observed on the west- tudinal ranges, i.e. with different altitudinal ranges, ern slopes of the Ghats, as shown by the mapping of pointing to the floristic homogeneity of the western species occurrences (Fig. 5b). slopes of the Ghats (Fig. 5b). At the positive end, are species whose distributions correspond to these middle elevation slopes, such as Litsea mysorensis and Hum- Environmental ranges of endemic species boldtia brunonis, whereas at the negative end, are two We then analyzed the role of environmental factors by kinds of species: 1) species whose distributions are assessing species niche differentiation along the three restricted to the coastal area, such as Buchanania lance- main environmental gradients. This was done by per- olata in the south and Garcinia indica in the north, and forming a CANCOR between the occurrences-by-spe- 2) species located on the top and/or the eastern slopes cies and occurrences-by-environment tables (cf. Fig. 3).

Fig. 5. Multispecies spatial patterns obtained by partial CCTSA removing the effect of environmental variables. Map- ping of occurrence canonical scores by contour curves computed over the 500 nearest neighbours, and projection of the occurrences of species characteristic of the spatial patterns identiﬁed. The colours reﬂect variation in occurrence scores (cf. insert). See Ap- pendix for species names.

434 ECOGRAPHY 26:4 (2003) The first two factors were highly significant, repre- tude and dry season length (Fig. 6b). The tips of this senting 87% of total variance (pB0.001). The canonical triangle are occupied by three kinds of species with a correlation coefficients were equal to 0.803 and 0.573. narrow ecological range: 1) species restricted to the The first factor represents the altitudinal gradient, lowlands with a short dry season, such as Myristica whereas the second factor corresponds to the gradient fatua var. magnifica and Gymnacranthera canarica,two of dry season length and, to a less extent, the rainfall species typically associated with swamps, 2) species gradient (Fig. 6a). On the first canonical plane, the restricted to the high elevations, such as the unique projection of species at the centroid of their occurrences species of Magnoliaceae Michelia nilagirica and of forms a triangle, showing the correlation between alti- Caprifoliaceae Viburnum hebanthum, and 3) species re-

Fig. 6. Results of CANCOR of occurrences-by-endemic tree species and occurrences-by-environment tables. a) correlation of the environmental variables with the ﬁrst two canonical factors, b) projection of species at the centroid of their occurrences. Species with the highest scores are represented by their names, with the other species represented by dots. See Appendix for species names.

ECOGRAPHY 26:4 (2003) 435 Fig. 7. Species environmental ranges within the most species-rich genera. a) Litsea; b) Diospyros;c)Syzygium. Species represented by ellipses containing 50% of their occurrences. See Appendix for species names.

stricted to the lowlands with a long dry season, such as medium elevation, D. nilagirica, and none occurs at Diospyros angustifolia and Garcinia indica. Between high elevation. The length of the dry season in addition these species, are species with a broader environmental to the amount of rainfall appears as the main factor of range, with the generalists located near the origin of the species niche differentiation. For example, the second canonical plane. canonical factor separates species tolerating a long dry season, such as D. angustifolia, from species inhabiting Species niche separation among congeneric species the lowlands under a short dry season, such as D. In order to assess the importance of species niche bourdillonii. Within this last group, it distinguishes D. separation among congeneric species, we plotted the foliolosa, a species located on the eastern side of the results separately for the three most species-rich genera, Ghats, where the annual rainfall is lower than on the Litsea (Lauraceae), Diospyros (Ebenaceae) and Syzy- western side. The highest niche overlap is observed at gium (Myrtaceae); the low number of species per genus low elevation under a short dry season. allowed the visualization of species niches by ellipses With 20 endemic species, Syzygium represents the containing 50% of their occurrences (Fig. 7). most species-rich genus of the endemic tree ﬂora of the Litsea species occupy most of the environmental Western Ghats, but the majority of its species are rare. space, displaying rather wide ecological amplitudes, Compared with the two previous genera, species niche except three species with a narrow altitudinal range, L. differentiation among the 8 most abundant Syzygium tra6ancorica, restricted to the lowlands, L. keralana, species is especially high (Fig. 7c). occurring at middle elevation, and L. wightiana var. tomentosa, inhabiting the tops of the mountains (Fig. Contribution of higher taxonomic ranks to species 7a); the highest niche overlap is observed at middle distribution elevation (800–1400 m) under medium dry season length (3–4 months). Species geographical and environmental ranges are ex- Contrary to Litsea, Diospyros is primarily located in pected to differ among genera and families, as these the lowlands (Fig. 7b). Only one species is observed at higher taxonomic ranks may be characterized by a

436 ECOGRAPHY 26:4 (2003) Table 1. Contribution of higher taxonomic levels to species of family is lower than the influence of genus. In terms ecological ranges. Canonical correlation coefficient (r) and percentage of total variance (% V) of the first two factors of patterns however, no difference is observed regard- compared for three analyses: CANCOR between the occur- ing species-environment relationships: niche separation rences-by-species and occurrences-by-environment tables (SE), along the environmental gradients occurs primarily and same analysis after partialling out the effect of genus within genera, i.e. at the species level. Regarding the (SE-G) or family (SE-F) (see text for further details). multispecies spatial patterns independent of environ- Axis AnalysisSE SE-G SE-F ment, slight differences are observed after removing the effect of genus (Figs 5 and 8). On the first factor, of the 1 r 0.803 0.651 0.756 % V57.85 59.48 58.52 three floristic regions identified previously, the south- 2 r0.573 0.453 0.539 eastern region remains unchanged whereas the others % V29.51 28.87 29.02 are less clear, being divided into different subregions (Fig. 8a). On the second factor, the pattern is almost unchanged, with the floristic homogeneity of the middle Table 2. Contribution of higher taxonomic levels to species elevation slopes being even more strongly underlined geographical ranges. Canonical correlation coefficient (r) and percentage of total variance (% V) of the first two factors than in the previous analysis (Fig. 8b). compared for three analyses: partial CCTSA removing the In order to compare the multispecies spatial patterns effect of environmental variables (Sxy), and same analysis within genera, we joined the canonical scores of con- after partialling out the effect of genus (Sxy-G) or family (Sxy-F) (see text for further details). generic species by a polygon (Fig. 9). The size of the polygon decreases with the overlapping of geographical Axis Analysis SxySxy-G Sxy-F ranges among congeneric species, whereas its shape reflects the diversity of species ranges (congeneric spe- 1r 0.483 0.392 0.459 %V 26.92 29.28 27.02 cies may have narrow latitudinal extents and/or narrow 2 r 0.466 0.356 0.444 longitudinal extents). Four types of patterns were iden- % V 25.06 24.24 25.29 tified: 1) genera represented by a large polygon, such as Diospyros, Garcinia and Syzygium, 2) genera with a large variance of species scores on the first factor, such series of traits influencing species dispersal capacities or as Actinodaphne, Goniothalamus and Symplocos, 3) gen- environmental tolerance. We analyzed the contribution era with a large variance of species scores on the second of genus and family to species ranges by means of factor, such as Litsea and Microtropis, and 4) genera partial CANCOR. If genera (or families) are not ran- represented by a small polygon, such as Psychotria. domly distributed, the results of these partial analyses These multispecies spatial patterns were visualized by should differ from the previous ones. mapping the occurrences of congeneric species with After partialling out the effect of genus or family on contrasted factorial scores. For instance, if one consid- species ranges, the canonical correlation coefficients ers the genus Actinodaphne, at the positive end of the decrease, indicating that these higher taxonomic levels first factor one finds A. angustifolia, a species occupying partly determine species environmental and geographi- the northern part of the Ghats, and A. campanulata cal ranges (Tables 1 and 2). In both cases, the influence var. campanulata, a species restricted to the southeast,

Fig. 8. Multispecies spatial patterns obtained by partial CCTSA removing the effect of environment and genus. Mapping of canonical scores by contour curves computed over the 500 nearest neighbours, and location of species within genera that have high and contrasted factorial scores. a) ﬁrst factor, b) second factor. The colours reﬂect variation in occurrence scores (cf. insert). See Appendix for species names.

ECOGRAPHY 26:4 (2003) 437 Fig. 9. Species factorial map obtained by a partial CCTSA removing the effect of environment and genus. The species represented at the centroid of their occurrences (black squares) are joined within each genus. The size of the polygon reﬂects the importance of spatial segregation among species belonging to the same genus. ACTI, Actinodaphne; AGLA, Aglaia; DIOS, Diospyros; EUON, Euonymus; GARC, Garcinia; GONI, Goniothalamus; LITS, Litsea; MALL, Mallotus; MICR, Microtropis; PSYC, Psychotria; SAPR, Saprosma; SYMP, Symplocos; SYZY, Syzygium.

while at the negative end one finds A. lawsonii, a species patterns obtained for both analyses were similar (Figs 6 restricted to the central part of the Ghats, essentially and 10). the Nilgiri Mountains, and A. tadulingami, a species Within the triangle formed by the projection of present both in the northern and in the central regions occurrences on the first canonical plane, the overlap of but absent from the southeastern area (Fig. 8a). If one family ecological profiles is not uniform and indicates considers the genus Litsea, at the positive end of the that most of the families are present at low to medium second factor one finds L. bourdillonii, L. floribunda, L. elevation under a short to medium dry season (Fig. keralana, L. ligustrina and L. mysorensis, five species 10b). The narrow profiles observed at the tips of the occupying the middle elevation slopes of the Ghats, triangle often correspond to ‘‘monospecific’’ families while at the negative end one flfinds L. glabrata, L. (i.e. families with only one tree species endemic to the wightiana var. tomentosa and L. wightiana var. Western Ghats), such as Caprifoliaceae, Ericaceae and wightiana, three taxa occurring on the tops of the Magnoliaceae at high elevation, and Apocynaceae, 6 Ghats, and L. tra ancorica, a species occupying the low Combretaceae and Rhizophoraceae at low elevation elevation slopes of the southern part of the Ghats under a short dry season. Conversely, the families (Fig. 8b). having the largest environmental profiles correspond to the most species-rich families, notably Euphorbiaceae, En6ironmental profiles of the endemic tree families Lauraceae and Rubiaceae, suggesting a link between Another way to assess the contribution of family to the clade diversification and species niche differentiation. observed species ranges is to analyze family environmental profiles. This was done by CANCOR of occurrences-by-families and occurrences-by-environment tables. The analysis produced two highly significant factors Discussion B representing 93% of total variance (p 0.001). As Distribution of endemism in the Western Ghats expected, the correlation between taxa and environment was lower for families than for species: the canonical The comparison of the pattern identified by the first correlation coefficients were 0.548 and 0.269. The factor of CCTSA (Fig. 4a) with variation in altitude

438 ECOGRAPHY 26:4 (2003) Fig. 10. Results of CANCOR of occurrences-by-families and occurrences-by-environment. a) correlation of the environmental variables with the ﬁrst two canonical factors, b) representation of the 38 families by ellipses containing 50% of their occurrences. Anac, Anacardiaceae; Anno, Annonaceae; Apoc, Apocynaceae; Aqui, Aquifoliaceae; Aral, Araliaceae; Arec, Arecaceae; Aste, Asteraceae; Capr, Caprifoliacae; Cela, Celastraceae; Clus, Clusiaceae; Comb, Combretaceae; Corn, Cornaceae; Dipt, Diptero- carpaceae; Eben, Ebenaceae; Elae, Elaeocarpaceae; Eric, Ericaceae; Euph, Euphorbiaceae; Faba, Fabaceae; Flac, Flacourtiaceae; Laur, Lauraceae; Magn, Magnoliaceae; Mela, Melastomataceae; Meli, Meliaceae; Mora, Moraceae; Myri, Myristicaceae; Myrs, Myrsinaceae; Myrt, Myrtaceae; Olea, Oleaceae; Pitt, Pittosporaceae; Rhiz, Rhizophoraceae; Rubi, Rubiaceae; Ruta, Rutaceae; Sapi, Sapindaceae; Sapo, Sapotaceae; Stap, Staphylaceae; Ster, Sterculiaceae; Symp, Symplocaceae; Thea, Theaceae.

(Fig. 2a) indicates that the change in endemic species Biogeographic history of the Western Ghats composition is mainly driven by the altitudinal gradient The analysis of family environmental proﬁles by CAN- and the related decrease in temperature, while the ho- COR can be interpreted in the light of the biogeo- mogenization of ﬂoristic composition observed in the northwestern part of the study area can be explained by graphic history of the Western Ghats. Indeed, the fact the effect of an increase in dry season length being that most of the families are present at low to medium counterbalanced by the effect of an increase in the elevation under a short dry season (Fig. 10) indicates amount of occult precipitation with elevation (Fig. 2b). that this habitat is associated with a larger pool of The second factor emphasizes the concentration of endemic evergreen species than high elevation areas or endemic species in the southeastern part of the Ghats lowlands with a long dry season, and this could be and the concomitant decrease of endemic species rich- related to its older age, as compared to the other ness along the altitudinal and the dry season length habitats (cf. Taylor et al. 1990). After the uplift of the gradients. Indeed, the steep gradient of b-diversity to- Western Ghats, wet evergreen taxa would have been wards the coast in the southern part, can be explained faced with a physiological barrier to occupy the new by a severe decrease of endemic species richness due to habitats, i.e. high elevation areas and lowlands with a the high anthropogenic pressure that characterizes the long dry season. As a consequence, the current latitudi- coastal area (Fig. 4b). nal and altitudinal gradients of endemic species richness

ECOGRAPHY 26:4 (2003) 439 (Fig. 4) could result from these historical and evolu- diate position of the slopes of the Ghats along the tionary factors. A similar hypothesis has been formu- altitudinal gradient. This allows the co-existence of lated by Latham and Ricklefs (1993) regarding the species from the lowlands or from the tops of the Ghats northern temperate tree flora. with species typical of middle elevation forests, a phe- The environmental profiles of the ‘‘monospecific’’ nomenon emphasized by the decrease in endemic spe- families can be related to the Quaternary history of the cies richness towards the coast and the tops of the Western Ghats. On the one hand, families restricted to Ghats (Fig. 4b). So the middle elevation slopes of the high elevation areas (\ 1800 m) have a Laurasian Ghats appear as an area of species accumulation rather affinity (cf. Raven and Axelrod 1974), so these species than a centre of speciation. most probably migrated from Himalaya during glacial periods and took refuge at the highest elevations of the Allopatric speciation Ghats, as postulated by Vishnu-Mittre (1974) for the The analysis of multispecies spatial patterns within Ericaceae Rhododendron nilagiricum (Fig. 10). Indeed, genera provides an insight into the origin of the three the Western Ghats experienced a cooler and drier cli- floristic regions. Indeed, the limits of the southeastern mate during the glacial cooling in the Quaternary (cf. region remain unchanged while the other regions be- Rostek et al. 1997). On the other hand, families re- come less clearly delimited (Fig. 8a). This result sug- stricted to low and middle elevations with a short dry gests a general phenomenon of geographical vicariance season have a Gondwanan affinity, so these species may for evergreen species between the eastern and the west- be relictual or recently evolved taxa, with the southern ern sides of the Ghats, whereas independent adapta- part of the Ghats representing a former refuge for tions to the long dry season would have occurred on species of the wet evergreen forest, or alternatively an the western side, as shown by the relative distributions active centre of speciation (cf. De Franceschi 1993). of Actinodaphne species (Fig. 8a). The phylogenetic Indeed, summer rainfall would have persisted in this analyses of Indian Sapotaceae and Ebenaceae by De region in the Quaternary (Van Campo 1986), and the Franceschi (1993) are consistent with the hypothesis of topographic complexity of the middle elevation reliefs allopatric speciation: Diospyros foliolosa and D. panicu- of the southern part of the Ghats could have favoured lata would derived from a widely distributed ancestor species survival as well as species formation (cf. Fjeldsa˚ that underwent differential selection on each side of the and Lovett 1997). Western Ghats.

Adapti6e radiation Speciation processes in the endemic tree flora of the The analysis of species environmental ranges reveals the Western Ghats importance of species niche separation along the altitudinal and the dry season length gradients (Fig. 6). This The analysis of multispecies spatial patterns by partial general feature holds among congeneric species, sug- CCTSA allowed the identification of three groups of species with a narrow latitudinal range that define three gesting a link between speciation and niche evolution. floristic areas, with the strongest floristic differentiation While altitude appears as the main factor of species observed between the southeastern and the central part niche separation within Syzygium (Fig. 7c), the length of the study area (Fig. 5a). Variation in the three of the dry season plays this role within Diospyros, environmental factors measured here shows that the primarily located at low elevation (Fig. 7b), and both northern region is characterized by a long dry season factors contribute to species niche separation within (Fig. 2b), while the central region is located around Litsea (Fig. 7a). The steepness of the environmental Palghat Pass, an interruption in the relief of the Ghats gradients in the Western Ghats could have favoured the isolating Nilgiri from Palni Mountains (Fig. 2a), and diversification of the evergreen tree flora by parapatric the southern region mainly corresponds to the eastern or sympatric speciation (cf. Endler 1982, Hodges and side of the Ghats, also characterized by a low total Arnold 1994, Schneider et al. 1999). annual amount of rainfall (Fig. 2c). So the existence of However, the comparison of congeneric species spa- distinct endemic floras can be explained by physical tial patterns shows that the hypothesized phenomena of and/or climatic barriers that would have limited species geographical and environmental vicariances have not migration or adaptation, also enhancing range contrac- affected all genera equally. Indeed, the six species of tion and species extinction processes. Psychotria have largely overlapping ranges, compared The second pattern identified by this analysis con- with the five species of Garcinia (Fig. 9). This means cerns the floristic homogeneity of the western slopes of that diversification of congeners is not necessarily corre- the Ghats, in contrast to the coastal area and the top of lated with species separation in physical or environmen- Palni and Nilgiri Mountains (Fig. 5b). As shown by the tal spaces. Several factors could explain these overlap in Litsea species ranges at middle elevation discrepancies. For instance, sympatric speciation could (Fig. 8b), this pattern seems to result from the interme- have occurred by polyploidy. An alternative hypothesis

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442 ECOGRAPHY 26:4 (2003) Appendix. List of species names identiﬁed by Canonical Correlation Analysis (Figs 5–8).

Species code Species name Family

actiangu Actinodaphne angustifolia (Bl.) Nees Lauraceae acticaca Actinodaphne campanulata var. campanulata J. Hk. Lauraceae actilaws Actinodaphne lawsonii Gamble Lauraceae actitadu Actinodaphne tadulingamii Gamble Lauraceae aglaelbo Aglaia elaeagnoidea (Juss.) Benth. var. bourdillonii (Gamble) Meliaceae K.K.N. Nair aglalawi Aglaia lawii (Wt.) Saldanha Meliaceae aporbour Aporosa bourdillonii Stapf. Euphorbiaceae ardirhom Ardisia rhomboidea Wt. Myrsinaceae bacccour Baccaurea courtallensis M. Arg. Euphorbiaceae bentcoda Bentinckia codapanna Berry Arecaceae blaccaly Blachia calycina Benth. Euphorbiaceae blacdenu Blachia denudata Benth. Euphorbiaceae blepmemb Blepharistemma membranifolia (Miq.) Ding Hou Rhizophoraceae buchlanc Buchanania lanceolata Wt. Anacardiaceae byrstetr Byrsophyllum tetrandrum (Bedd.) J. Hk. ex Bedd. Rubiaceae cantnene Canthium neilgherrense Wt. var. neilgherrense Rubiaceae casewyna Casearia wynadensis Bedd. Flacourtiaceae cinnripa Cinnamomum riparium Gamble Lauraceae cinnwigh Cinnamomum wightii Meissn. Lauraceae cleimala Cleistanthus malabaricus M. Arg. Euphorbiaceae diosangu Diospyros angustifolia (Miq.) Kosterm. Ebenaceae diosassi Diospyros assimilis Bedd. Ebenaceae diosbarb Diospyros barberi Ramas. Ebenaceae diosbour Diospyros bourdillonii Brand. Ebenaceae dioscand Diospyros candolleana Wt. Ebenaceae diosfoli Diospyros foliolosa Wall. ex DC. Ebenaceae diosghat Diospyros ghatensis Ramesh & De Franceschi Ebenaceae dioshumi Diospyros humilis Bourd. Ebenaceae diosnila Diospyros nilagirica Bedd. Ebenaceae diospani Diospyros paniculata Dalz. Ebenaceae diosprur Diospyros pruriens Dalz. Ebenaceae diossald Diospyros saldanhae Kosterm. Ebenaceae diptbour Dipterocarpus bourdilloni Brandis Dipterocarpaceae drypconf Drypetes confertiflorus (J. Hk.) Pax & Hoffm. Euphorbiaceae elaerecu Elaeocarpus recur6atus Corner Elaeocarpaceae eugemacr Eugenia macrosepala Duthie Myrtaceae euonangu Euonymus angulatus Wt. Celastraceae euoncren Euonymus crenulatus Wall. ex Wt. & Arn. Celastraceae flacmont Flacourtia montana Grah. Flacourtiaceae garcindi Garcinia indica (Thouras) Choisy Clusiaceae garctrav Garcinia tra6ancorica Bedd. Clusiaceae garcwigh Garcinia wightii T. Andr. Clusiaceae glocbour Glochidion bourdillonii Gamble Euphorbiaceae glocjohn Glochidion johnstonei J. Hk. Euphorbiaceae glocneil Glochidion neilgherrense Wt. Euphorbiaceae gluttrav Gluta tra6ancorica Bedd. Anacardiaceae gonirhyn Goniothalamus rhynchantherus Dunn. Annonaceae gordobtu Gordonia obtusa Wall. ex Wt. & Arn. Theaceae gymncana Gymnacranthera canarica (King) Warb. Myristicaceae holibedd Holigarna beddomei J. Hk. Anacardiaceae homatrav Homalium tra6ancoricum Bedd. Flacourtiaceae hopepong Hopea ponga (Dennst.) Mabb. Dipterocarpaceae hoperaco Hopea racophloea Dyer Dipterocarpaceae hopeutil Hopea utilis (Bedd.) Bole Dipterocarpaceae humbbrun Humboldtia brunonis Wall. Fabaceae humbdecu Humboldtia decurrens Bedd. ex Oliv. Fabaceae humbvahl Humboldtia 6ahliana Wt. Fabaceae hydnmama Hydnocarpus macrocarpa Bedd. Warb. ssp. macrocarpa Flacourtiaceae isonperr Isonandra perrottetiana DC. Sapotaceae ixornoto Ixora notoniana Wall. ex G. Don. Rubiaceae ixorpoly Ixora polyantha Wt. Rubiaceae lasirost Lasianthus rostratus Wt. Rubiaceae litovenu Litosanthes 6enulosus (Wt. & Arn.) Deb. & Gang. Rubiaceae litsbour Litsea bourdillonii Gamble Lauraceae litscori Litsea coriacea J. Hk. Lauraceae litsflor Litsea floribunda Gamble Lauraceae litsglab Litsea glabrata J. Hk. Lauraceae litskera Litsea keralana Kosterm. Lauraceae

ECOGRAPHY 26:4 (2003) 443 Appendix. (Continued).

Species code Species name Family

litslaev Litsea lae6igata Gamble Lauraceae litsligu Litsea ligustrina J. Hk. Lauraceae litsmyso Litsea mysorensis Gamble Lauraceae litsstoc Litsea stocksii J. Hk. Lauraceae litstrav Litsea tra6ancorica Gamble Lauraceae litswito Litsea wightiana (Nees) J. Hk. var. tomentosa Meissn. Lauraceae litswiwi Litsea wightiana (Nees) J. Hk. var. wightiana Lauraceae mallatro Mallotus atro6irens J. Hk. Euphorbiaceae mammsuri Mammea suriga (Buch.-Ham. ex Roxb.) Clusiaceae maytroth Maytenus rothiana (Walp.) Ramam. Celastraceae memeheyn Memecylon heyneanum Benth. ex Wt. & Arn. Melastomataceae memetalb Memecylon talbotianum Brandis Melastomataceae michnila Michelia nilagirica Zenk. Magnoliaceae micrmicr Microtropis microcarpa Wt. Celastraceae myrifama Myristica fatua Houtt. var. magnifica (Bedd.) Sinclair Myristicaceae neolfisc Neolitsea fischeri Gamble Lauraceae ochrmiss Ochrinauclea missionis (Wall. ex G. Don.) Ridsd. Rubiaceae octotrav Octotropis tra6ancorica Bedd. Rubiaceae ormotrav Ormosia tra6ancorica Bedd. Fabaceae palabour Palaquium bourdilloni Brand. Sapotaceae phaemala Phaeanthus malabaricus Bedd. Annonaceae pithgrac Pithecolobium gracile Bedd. Fabaceae pittdasy Pittosporum dasycaulon Miq. Pittosporaceae pittneel Pittosporum neelgherrense Wt. & Arn. Pittosporaceae popobedd Popowia beddomeana J. Hk. & Thoms. Annonaceae psycdalz Psychotria dalzellii J. Hk. Rubiaceae psycglob Psychotria globicephala Gamble Rubiaceae psycnudi Psychotria nudiflora Wt. & Arn. Rubiaceae psyctrun Psychotria truncata Wall. Rubiaceae pterreti Pterospermum reticulatum Wt. & Arn. Sterculiaceae pterrubi Pterospermum rubiginosum Heyne ex Wt. & Arn. Sterculiaceae rhodnila Rhododendron nilagiricum Zenk. Ericaceae sagegran Sageraea grandiflora Dunn. Annonaceae sagelaur Sageraea laurifolia (Grah.) Blatt. & Mc. Cann. Annonaceae saprcory Saprosma corymbosum Bedd. Rubiaceae schecapi Schefflera capitata (Wt. & Arn.) Harms Araliaceae scherace Schefflera racemosa Harms Araliaceae semeauri Semecarpus auriculata Bedd. Anacardiaceae semetrav Semecarpus tra6ancorica Bedd. Anacardiaceae sympfoli Symplocos foliosa Wt. Symplocaceae sympmama Symplocos macrocarpa Wt. ex Cl. ssp. macrocarpa Symplocaceae sympmaro Symplocos macrophylla Wall. ex A. DC. ssp. rosea (Bedd.) Noot. Symplocaceae sympwyna Symplocos wynadense (O. K.) Noot. Symplocaceae syzybent Syzygium benthamianum (Wt. ex Duthie) Gamble Myrtaceae syzydens Syzygium densiflorum Wall. ex Wt. & Arn. Myrtaceae syzylaet Syzygium laetum (Buch.-Ham.) Gandhi Myrtaceae syzymala Syzygium malabaricum (Bedd.) Gamble Myrtaceae syzymund Syzygium mundagam (Bourd.) Chithra Myrtaceae syzyocci Syzygium occidentale (Bourd.) Gandhi Myrtaceae syzyrama Syzygium rama-6arma (Bourd.) Chithra Myrtaceae syzytami Syzygium tamilnadensis Rathak. & Chithra Myrtaceae tabegamb Tabernaemontana gamblei Subramanyam & Henry Apocynaceae termtrav Terminalia tra6ancorensis Wt. & Arn. Combretaceae verntrav Vernonia tra6ancorica J. Hk. Asteraceae vibuheba Viburnum hebanthum Wt. & Arn. Caprifoliaceae

444 ECOGRAPHY 26:4 (2003)