a multivariate approach to assess the taxonomic utility of morphometric characters in doronicum...

A Multivariate Approach to Assess the Taxonomic Utility of Morphometric Characters inDoronicum (Asteraceae, Senecioneae)Author(s): Inés Álvarez Fernández and Gonzalo Nieto FelinerSource: Folia Geobotanica, Vol. 36, No. 4 (2001), pp. 423-444Published by: SpringerStable URL: http://www.jstor.org/stable/25133857 .

Accessed: 17/06/2014 13:01

Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at .http://www.jstor.org/page/info/about/policies/terms.jsp

.JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range ofcontent in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new formsof scholarship. For more information about JSTOR, please contact [email protected].

.

Springer is collaborating with JSTOR to digitize, preserve and extend access to Folia Geobotanica.

http://www.jstor.org

This content downloaded from 62.122.79.81 on Tue, 17 Jun 2014 13:01:25 PMAll use subject to JSTOR Terms and Conditions

http://www.jstor.org/action/showPublisher?publisherCode=springer

http://www.jstor.org/stable/25133857?origin=JSTOR-pdf

http://www.jstor.org/page/info/about/policies/terms.jsp


Folia Geobotanica 36: 423-444, 2001

A MULTIVARIATE APPROACH TO ASSESS THE TAXONOMIC UTILITY OF MORPHOMETRIC CHARACTERS IN DORONICUM

{ASTERACEAE, SENECIONEAE)

Ines Alvarez Fernandez & Gonzalo Nieto Feliner

Real Jardin Botdnico, CSIC, Plaza de Murillo 2, E-28014 Madrid, Spain; fax +34 914200157,

e-mail [email protected]

Keywords: Discriminant analysis, Ordination techniques, Principal components analysis, Taxonomy

Abstract: A multivariate morphometric study based on 22 characters was carried out on samples of the 26

accepted species of the Eurasian and north-African genus Doronicum, to assess whether quantitative, mainly

continuous, characters were of use in suggesting, delimiting and structuring natural groups. The study

concentrated on three-medium sized to small groups: Mediterranean (D. plantagineum group), European

(D. grandiflorum group), and central Asian. Two questions were addressed for each of these groups: species

delimitation within them and the inclusion/exclusion of species of uncertain, but putative close affinities.

Principal components analysis and discriminant analysis (canonical variates analysis), gave moderately

satisfactory results. The addition of doubtfully-related species to presumably natural groups increased

cohesiveness of the groups because the between-species differences were minimized when placed in a broader

more diverse context. The relative status of the uncertain species, either as outliers or true members, was

appropriately depicted by the scatterplots, but more convincingly solved when the species turned out to be

outliers. Discrimination between species, which belong to cohesive groups was effective in some cases at least

when using discriminant analysis, and the exceptions involved particularly problematic taxa. It was concluded

that morphometric characters are a useful complementary source of information in groups where qualitative (in

particular, shared) characters are scarce as is the case in Doronicum.

INTRODUCTION

The genus Doronicum (Asteraceae, Senecioneae) is represented by perennial rhizomatose

herbs with alternate, simple leaves, bearing one to several radiate yellow-flowered capitula.

Phyllaries are all uniform, herbaceous, and arranged in 2-3 rows. Cypselae are broadly

elliptic-oblong and have 10 longitudinal ribs. A pappus of bristles is present in all cypselae,

except for the ligulate florets of the heterocarpic species, where it is lacking. The

representatives of this genus are distributed in Asia, Europe, and northern Africa, and occur on

open or forested habitats from sea level up to 5,000 m of elevation.

Although several taxonomic studies of the genus Doronicum circumscribed to particular

regions are available (Widder 1925, Edmondson 1973, 1975, 1978, Avetisjan 1980,

Chacon 1987, Perez Morales & Penas 1990, Duvigneaud 1992, Perez Morales et al.

1994), the only comprehensive revision of this genus is that by Cavillier (1907, 1911). He

recognized 34 species arranged in 3 sections: Doronicastrum Cavill., Soulieastrum Cavill.,

and Hookerastrum Cavill. The latter section included one species nowadays placed in another

genus within a different tribe, Nannoglottis hookeri (C.B. Clarke ex Hook, f.) Kitam. While

sect. Soulieastrum is monospecific (D. stenoglossum Maxim.), Cavillier subdivided his main



424 |. Alvarez Fernandez & G. Nieto Feliner

Table 1. Outline of the taxonomy of the genus Doronicum proposed in ALVAREZ FERNANDEZ (1999). Informal

groups, mainly based on morphology and geography, are considered instead of formal infrageneric categories. - in Alvarez Fernandez & Nieto Feliner (2000);2

- in Alvarez Fernandez (2001).

Group Taxa

D. cavillieri ALVAREZ FERNANDEZ et NlETO FEL. l

D. kamaonense (DC.) ALVAREZ FERNANDEZ 2

(D. roylei DC.) D. oblongifolium DC.

D. pardalianches L.

D. stenoglossum MAXIM.

D. austriacum group D. austriacum JaCQ. D. carpetanum BOISS. et REUT. ex WlLLK. subsp. carpetanum D. carpetanum subsp. diazii (PEREZ MORALES et PENAS) ALVAREZ FERNANDEZ

2

D. carpetanum subsp. kuepferi (R. CHACON) ALVAREZ FERNANDEZ 2

D. carpetanum subsp. pubescens (PEREZ MORALES, PENAS, LLAMAS et ACEDO) AIZPURU

D. cataractarum WlDDER

D. corsicum (LOISEL.) POIR.

D. plantagineum group D. carpaticum (GRISEB. et SCHENK) NYMAN

D. columnae TEN.

D. hungaricum RCHB. f.

D. orientate HOFFM.

D. plantagineum L. (D. atlanticum CHABERT)

SW Asian group D. cacaliifolium BOISS. et HELDR.

D. dolichotrichum CAVILL.

D. haussknechtii CAVILL.

D. macrophyllum FlSCH. subsp. macrophyllum (D. macrolepis FREYN et SlNT.) D. macrophyllum subsp. sparsipilosum (J.R. EDM.) ALVAREZ FERNANDEZ

2

D. maximum BOISS. et A. HUET

D. reticulatum BOISS.

Central Asian group D. altaicum PALL.

D. briquetii CAVILL.

D.falconeriC.B. CLARKE (A turkestanicum CAVILL.)

D. grandiflorum group D. grandiflorum LAM.

D. clusii (ALL.) TAUSCH

D. glaciate (WULFEN) NYMAN_

section, Doronicastrum, into 7 subsections. This treatment needed a thorough revision since

the subsections are not defined on the basis of exclusive (synapomorphic) characters, and

since the variability of those characters used to define subsections actually extends far beyond

the limits of his subsections (e.g., leaf size and shape, plant size, number of capitula). As a

consequence, the placement of several species within Cavillier's treatment is rather arbitrary

as is the circumscription of most of his subsections.

A taxonomic revision of the genus based on ca. 4,500 herbarium specimens from 47

herbaria has resulted in a new taxonomic treatment (Alvarez FernAndez 1999, 2001,

Alvarez FernAndez & Nieto Feliner 1999, 2000), which recognizes 26 species and

4 subspecies.



Morphometric characters in Doronicum 425

Taxonomy is problematic, in part due to the scarcity of putative synapomorphies (primary homologies sensu De Pinna 1991) within the genus. From a raw matrix of 44 characters (not

shown), only ten could be selected as potentially informative for a phylogenetic analysis (Alvarez FernAndez et al. 2001). This reduction resulted from the removing of quantitative continuous characters, autapomorphies, intra-taxon polymorphic characters, and those which,

despite superficial similarity, were presumably non-homologous. Even after this previous selection, only three of the remaining ten characters contained no homoplasy in a simultaneous

(total evidence) parsimony analysis based on three different data sets: morphology, nuclear ribosomal ITS DNA sequences, and chloroplast tmL-tmF sequences (Alvarez FernAndez et al. 2001). These were the ciliate phyllaries, the scapose stem, and the triplinerved leaf venation. These three characters support the recognition of the D. plantagineum group (Tab. 1). The simultaneous analysis of the three data sets constitutes a homology test for each

character against the rest in the data set (Patterson 1988). The remaining seven characters contained different amounts of homoplasy, and thus failed a test of homology by congruence

with other characters: homocarpy, the presence of hairs and buds in the rhizome, the shape and

arrangement of nodes and internodes in the rhizome, the pinnate-reticulate leaf venation, the

plant architecture displayed by the SW Asian species (a few scattered very large leaves and several capitula), and the glandular cypselae. As a consequence of the low reliability of

morphological characters at the above-species level, infrageneric taxa are not recognized, but several informal groups of species are named and are referred to below and in Tab. 1.

To a lesser extent, problems also exist at lower taxonomic levels. Species delimitation is, in a few cases, based on autapomorphic morphological characters. However, most of the species are defined by combinations of non-exclusive characters. The fact that some of these are continuous and their ranges of variation are wide can make species recognition equivocal.

Given the paucity of qualitative characters in Doronicum, and their questionable reliability for delimiting natural groups, we decided to assess whether quantitative, primarily continuous, characters were useful for taxonomic purposes. The objective of the present paper is thus to determine if morphometric multivariate patterns of variation can help in suggesting, delimiting and structuring natural groups. For operability, we have chosen three smaller

groups of species that are presumably natural and involve unresolved taxonomic problems. In

particular, two different questions have been addressed based on those groups: species delimitation within them and the inclusion/exclusion of species of uncertain affinities in these selected groups.

MATERIAL AND METHODS

Plant material and data sets

A total of 291 specimens were scored from the following herbaria: B, BM, BRNM, E, G, GAZI, GH, GZU, K, LE, MA, MO, NY, and W. The origin of the material is given in Appendix 1. These specimens are representatives of the 26 species and 4 subspecies recognized in our taxonomic treatment (Alvarez FernAndez 1999). An outline of such treatment as well as

authorship of the taxa are given in Tab. 1. However, to allow visualization and discussion of their morphometric behavior, specimens representing two previously recognized species that

we consider synonyms have been labeled separately. These are D. atlanticum and D. turkestanicum, synonyms of D. plantagineum and D.falconeri, respectively. For most of



426 I. Alvarez Fernandez & G. Nieto Feliner

the taxa, ten specimens spanning its geographic distribution were selected, sometimes

including all the available material.

A global matrix including all the samples was used in a preliminary analysis. Even though it

is likely to provide only a coarse picture of morphometric variation for taxonomic purposes, this matrix was analyzed to determine if there is a general pattern of variation that is consistent

with any of the infrageneric arrangements proposed. To facilitate examination of the

scatterplot, only five species were labeled independently (D. stenoglossum, D. oblongifolium, D. cavillieri, D. pardalianches, D. kamaonense), D. kamaonense being the correct name for

D. roylei (Alvarez Fernandez 2001). These five species are either morphologically very

distinct or cannot be included in other groups with certainty. The rest of the species were

gathered for labeling under five different groups based on morphological characters recorded

during the taxonomic revision (Tab. 1). The species included in those groups share

morphological, geographical and often ecological features, although they do not necessarily

represent natural groups.

These groups are: (1) D. austriacum group: European tall herbs with leafy stem and several

capitula. It includes D. austriacum, D. carpetanum (subsp. carpetanum, subsp. diazii, subsp.

kuepferi, and subsp. pubescens), D. cataractarum, and D. corsicum. (2) D. plantagineum

group, including European taxa with ciliate phyllaries, scapose stem, and triplinerved leaf

venation. It is a seemingly natural group constituted of D. hungaricum, D. orientate,

D. plantagineum, D. carpaticum, and D. columnae. Because D. carpaticum and D. columnae

are not core members, we refer to the remaining three species as D. plantagineum s. str. group.

(3) SW Asian group: species from Asia Minor, Caucasus, and Iran, integrated by tall herbs

with a few very large cauline leaves, and several to many capitula. It includes D. cacaliifolium, D. dolichotrichum, D. haussknechtii, D. macrophyllum (subsp. macrophyllum and subsp.

sparsipilosum), D. maximum, and D. reticulatum. (4) Central Asian group, integrated by

species with one capitulum (very rarely up to four), leaves scattered along the stem,

pinnate-reticulate venation and numerous ligulate florets (30). It includes D. altaicum,

D. briquetii and D.falconeri. (5) D. grandiflorum group, integrated by homocarpic European

short herbs with one capitulum and several leaves scattered along the stem, occurring in open

mountain areas. It includes D. grandiflorum, D. clusii, and D. glaciale. Three of these groups were selected for further analyses based on three criteria: they were

presumably monophyletic, they stand as one of the putative closest relatives to species whose

placement was doubtful, and/or they involved internal taxonomic problems that could be

addressed with multivariate techniques. These were the D. plantagineum group (no. 2), the

D. grandiflorum group (no. 5), and the central Asian group (no. 4). Two species of uncertain

affinities (D. carpaticum and D. columnae) were analyzed with the first two groups, while

another three (D. cavillieri, D. kamaonense and D. stenoglossum) were included in the third.

Characters

Since floral and fruit characters are not shown simultaneously in the same specimen, we

were forced to exclude all characters relative to the cypselae except for the occurrence of

heterocarpy, which can be easily visualized by the absence of a pappus in the ligulate florets.

Most of the measurements were made with a Brown & Sharpe Plus digital calliper (model

599-571-3).




Table 2. Characters scored for the multivariate analyses (DA and PCA). All distance measures are in mm except for LT. Number in parentheses denote coding of discrete characters.

1. ABE: phyllary maximum width

2. AMP: receptacle base width

3. CAL: ratio of medium cauline leaf width to medium cauline leaf length 4. CALBE: ratio of phyllary maximum width to phyllary length 5. CALL: ratio of ligule maximum width to total ligulate floret length 6. CBL: ratio of phyllary length to ligulate floret length 7. CHB: ratio of basal leaf maximum width to basal leaf length 8. CLMLB: ratio of phyllary length (from the base to the maximum width) to phyllary total length 9. CLPLT: ratio of peduncle length (uppermost leafless portion of the stem) to stem length

10. CPL: ratio of basal leaf petiole length to basal leaf blade length 11. DIAM: diameter of the capitulum (phyllaries and ligulate florets excluded) 12. HB: basal leaves absent (0) vs. present (1) at flowering 13. HET: homocarpic capitulum (0), heterocarpic capitulum (1) 14. LA: anther length 15. LF: disk floret length 16. LHCM: medium cauline leaf length 17. LL: ligulate floret length 18. NC: number of capitula 19. NDA: number of teeth at the ligule apex

20. NEN: number of intemodes in the stem

21. NL: number of ligulate florets per capitulum 22. LT: stem length (categorized into three states < 0.6 m, 0.6-1 m, > 1 m)

On the whole, twenty-two characters were scored (Tab. 2). However, depending on the

group analyzed, some characters were not considered due to a lack of variation or the

inapplicability for the matrix in question. For instance, when analyzing the global matrix eight characters that could not be measured in all the 30 taxa were eliminated. The characters removed from each analysis due to the above reasons are given under the results section. As a consequence, the number of characters scored varied from 14 to 20. Eight of them are

quantitative continuous, another eight are ratios, four are quantitative discrete and two are

binary (homocarpy vs. heterocarpy, presence of basal leaves at flowering). One of the

quantitative continuous variables (stem length, LT) could not be measured exactly in

incomplete large herbarium specimens and was therefore categorized into three different states

(< 0.6 m, 0.6-1 m, > 1 m). The values in the data matrices are averages of the three measurements in each specimen except for CHB, CLPLT, CPL, DIAM, HB, HET, NC, NDA, NEN, NL, LT.

Analyses

Principal components analyses (PCA), based on the correlation matrix (Sneath & Sokal

1973, Abbott et al. 1985, Marcus 1990), were performed in order to see whether data reduction obtained through the new set of variables (PCs) revealed a pattern of variation that is consistent with the taxonomy. Although these analyses are not designed for grouping, clusters can be produced when the largest components of the overall variance are contributed by differences among groups.




CNJ 4T-1 o Q_ v

^ a a. v ?). cavillieri

t. . "'^.a-/ a** a? vn^ * D. kamaonense

^ 7 //1 *?^J^ ?** * ?3d*7

+ a pardalianches

T xA*A2 *^A+oSr^ v^7 * D stenoglossum

-1? xa ? -j?*1-^ q, ^ +

+8p&* v 7

v^ D D' austnacum group

-2 x ? a?

? a o. grandiflorum group

* v * D. plantagineum group "3" * Central Asian group

^ ? SW Asian group i- - -1- -??-a-i -3-2-10123

PC1 Fig. 1. Principal components analysis of the genus Doronicum. Scatterplot of 291 specimens against the first

two principal components axes. See text for explanation of the groups.

Discriminant analysis (DA) was used mainly as an ordination procedure, i.e., what is

sometimes called canonical variates analysis (Abbott et al. 1985, Marcus 1990). It was used

to check if specimens from each species could be discriminated efficiently from congeners on

the basis of morphometric characters when plotted against the canonical discriminant

functions that maximize between-group variation relative to within-group variation.

A stepwise procedure was followed to select the combination of variables that maximize the

discrimination of predetermined groups. The low number of specimens per group could cause

problems of degrees of freedom when using ca. 20 variables, although any number of variables

below the total number of specimens minus the number of groups is acceptable for other

authors (Klecka 1980). Since the number of variables selected by the stepwise procedure was

in all the analyses three to four, we avoided technical problems of this type. The selected

variables in each of the analyses are indicated under the results section. Besides the ordination, we have also used the classificatory approach of the DA. This uses a different set of

discriminant functions as compared to the canonical ones with which the scatterplots are

drawn. The percent of "correctly" classified specimens was obtained by the stringent

procedure of cross-validation. To refine the classification results, probabilities of pertaining to

each group for every specimen were also examined although they are not given in this paper. All the analyses were carried out using SPSS 10.0.5 for Windows.

RESULTS

Global matrix PCA

Characters excluded from this analysis are CAL, CHB, CLPLT, CPL, HB, LA, LHCM, and

NEN (Tab. 1). The first three PCs explain 56% of the variance (25%, 20%, and 11%,

respectively). Nine PCs are needed to account for 90% of the overall variance. The highest

loadings on the 1st PC correspond to characters CALBE, CLMLB, and ABE. This component




is related with phyllaries shape. The variables with the highest loadings on the 2nd PC are

DIAM, AMP, and LL. These variables are related with the appearance and size of the capitula. In the scatterplot of the 291 specimens against the first two PCs, no discrete clusters are

apparent (Fig. 1). Nonetheless, an examination of the placement of each species and group reveals a clear trend determined by the variables contributing most to the first two PCs.

Specimens with narrow acuminate phyllaries are on the left side of the plot, corresponding to

negative values for the PCI (D. plantagineum group, D. stenoglossum, D. pardalianches, and most of the central Asian group). Species presenting wide phyllaries are placed on the other extreme of the plot (most of the D. austriacum group, most of the SW Asian group, and

D. oblongifolium). The remaining species (D. kamaonense and the D. grandiflorum group) appear on the central portion of the plot.

Doronicum plantagineum group

Characters excluded from the analyses of this group are CAL, CHB, CPL, HB, LA, and LHCM (Tab. 1). The first three PCs explain 54% of the variance (23%, 17%, and 14%,

respectively). Ten PCs are needed in order to explain 90% of the overall variance. The variables with highest loadings on the 1st PC are LT, DIAM, and AMP. This component is related to the size of the plant and the capitula. The variables with the highest influence on the 2nd PC are CLPLT, NEN, and LL. These mostly depict plant architecture.

In the scatterplot against the first two PCs, no clear-cut clusters are apparent except maybe for the samples of D. orientale located towards the negative values for PC2 (Fig. 2A). The

specimens belonging to D. carpaticum and D. columnae occur on the upper left quadrant, partially overlapping with the remaining three species (D. atlanticum, D. hungaricum, and

D. plantagineum), which tend to cluster at the upper right quadrant. In the discriminant analysis, four variables were selected using the stepwise procedure

(NEN, LT, LF, LL). The first two canonical discriminant functions account for 94% of the

variance, the first of them being highly (negatively) correlated with NEN and the second with LT Classification results yielded 43 cases out of 59 (73%) assigned to the correct group when six groups are considered. When confusions within D. plantagineum (i.e., between specimens labeled as such and as "D. atlanticum") are excluded, the number of correctly-classified specimens increases to 48. Four of the 11 misclassifications involve confusions between

D. carpaticum and D. columnae. The remaining 7 involve confusions between D. carpaticum or D. columnae and one of the three species in the D. plantagineum group. In the scatterplot against the first two canonical discriminant functions, specimens belonging to D. columnae and D. carpaticum are largely overlapped (Fig. 2B), as are those previously recognized as

D. atlanticum with respect to the remaining D. plantagineum. The core members of the D. plantagineum group are not clearly separated from D. columnae and D. carpaticum.

Doronicum plantagineum s. str. group

Characters excluded from the analyses of this group are CAL, HB, HET, LA, and LHCM

(Tab. 1). The variance explained by the first three PCs is 59% (26%, 18%, and 15%,

respectively). Eight PCs are needed in order to explain 90% of the overall variance. The

highest loadings on the 1st PC correspond to CLPLT, NL, CHB and NEN. Therefore, the first

component is related mainly with plant architecture and the shape of the basal leaves. The




- _ _

CM 2 A

o M ?

* *o D. columnae 0 /s

^ D. carpaticum

D * . O D. hungaricum -1 + o

oa + D *

a D. orientate D

D + D. plantagineum -2 ?a "D. atlanticum"

* D. plantagineum

-3 -3-2-10123

PC1

l s I _ CM 4

B LL O Q "

O 3

?^ +

* * 2 O * ~

A o * . D. columnae

O * * n * + ? + D. carpaticum

o o +

O D. hungaricum I aa

-1 ? a a DO. orientate

' a a + D. plantagineum

oa "D. atlanticum" D a * D. plantagineum

-4 -4-20246

DF1

Fig. 2. Morphometric multivariate analysis of the Doronicum plantagineum group (including!), columnae and

?>. carpaticum). A - principal components analysis: scatterplot of the specimens against the first two principal

components axes. B - discriminant analysis: scatterplot of the specimens against the first two canonical

discriminant functions.

variables with the highest loadings on the 2nd PC are mainly related to the capitula appearance

(ABE and LF). In the scatterplot against the first two PCs, specimens are arranged in very loose and slightly

overlapped clusters (Fig. 3A). The most distinct is formed exclusively by D. hungaricum on

the lower right corner of the plot. The specimens belonging to D. orientale although rather

dispersed and adjacent to the remaining two species, are confined to the space with negative

values for the PCI. The samples of D. plantagineum show wide overlapping with their

conspecifics labeled as "?>. atlanticum'.




CM 'J *^ l A o + *

Q- + +

1 D D ? D

n *+ 0 D ? * *

* O D. hungahcum

o a D. orientate

D o ?

o +0. plantagineum "D. atlanticum"

? ? * D. plantagineum _o_

-2 -3-2-10 1 2

PC1

3 + + _*

?! B Q

*

2 + w* + *+

* + ^+ *

i" *

D 0 D + * * O ?

o o o

'a o

D a O D. hungaricum

a D. orientate

a + D. plantagineum

3*

D o "D. atlanticum"

* D. plantagineum

-41 " '-"-"-'

^4-20246

DF1 Fig. 3. Morphometric multivariate analysis of the Doronicum plantagineum s. str. group. A -

principal

components analysis: scatterplot of the specimens against the first two principal components axes. B -

discriminant analysis: scatterplot of the specimens against the first two canonical discriminant functions.

The variables remaining in the discriminant analysis after the completion of the stepwise procedure were the same (NEN, LT, LF, LL) as for the group enlarged to include also

D. columnae and D. carpaticum (D. plantagineum group). The first two canonical

discriminant functions account for 96% of the variance, the first of them being highly correlated with NEN and the second with LT, as in the D. plantagineum group. Classification

results yielded 35 cases (90%) assigned to the correct group. The four misclassifications

involved confusions between "D. atlanticum" and D. plantagineum. Therefore, 100% of the

specimens were classified into the predetermined species when our taxonomy (Tab. 1) is




CM 2 +

~

g * ? * A

1 ? * 1

. +.

*** ' ?

1 " **"

a a " ? + D. glaciate

o +

a < D * D. clusii

\ + D + .1 a n D. grandiflorum

D a o. columnae

m

A_*_ D. carpaticum

-2 -2-10 1 2 3

PC1

s: 5l I b 4 3 D

1 Q D

1 '

.* 1 D + 1

." A \ + D. glaciate J

A + + *Q

0| /aabA a * D * D. C/t/Sf/

J + * d D. grandiflorum -1

J **.+ +-** D. columnae

I + *

"2 D. carpaticum

-3 -6-4-2 0 2 4

DF1 Fig. 4. Morphometric multivariate analysis of the Doronicum grandiflorum group together with ?>. columnae

and ?>. carpaticum. A - principal components analysis: scatterplot of the specimens against the first two

principal components axes. B - discriminant analysis: scatterplot of the specimens against the first two

canonical discriminant functions.

followed. The scatterplot arranges the specimens into three loose groups corresponding to

D. hungaricum, D. orientale, and D. plantagineum (Fig. 3B).

Doronicum grandiflorum group plus D. carpaticum and D. columnae

Characters excluded from the analyses of this group are CHB, CPL, LA, and LHCM

(Tab. 1). The first three PCs explain only 49% of the variance (22%, 14%, and 13%,

respectively). Eleven PCs are needed to explain 90% of the overall variance. The highest




loadings on the 1st PC correspond to characters DIAM, AMP, LF, and ABE. This component is related to the size and the appearance of the capitula. Variables CALL, LL, and LT

contribute the most to the 2nd PC. This component is thus related to the size and the shape of

ligulate florets and to plant size. In the scatterplot against the first two PCs, discrete clusters are lacking (Fig. 4A). However,

most of the samples of D. carpaticum and D. columnae are placed on the left half of the space defined by the first two PCs, corresponding to negative values for PCI. The species of the

D. grandiflorum group overlap on the central and right areas.

Four variables remained in the discriminant analysis after the completion of the stepwise

procedure (LF, CAL, ABE, LT). The first two canonical discriminant functions account for

96% of the variance, the first of them being highly correlated with LF and the second with

CAL. Only 29 of the 50 specimens (58%) were correctly classified, and 20 of the 21

misclassifications involved confusions between D. carpaticum and D. columnae or between

D. grandiflorum, D. clusii andZ). glaciale, that is, only one crosses the borders of the two clear

subgroups recognizable in this analysis (D. carpaticum + D. columnae, on one side, the

D. grandiflorum group on the other). Furthermore, the second most likely group for all the 50

specimens did not cross the borders of the two subgroups either. The scatterplot against the

first two canonical discriminant functions provides a good synthesis of this result, i.e.

D. carpaticum and D. columnae widely overlapped and separated from the three species of the

D. grandiflorum group, which are also overlapped among themselves (Fig. 4B).

Central Asian group plus D. cavillieri, D. kamaonense and D. stenoglossum

Characters excluded from the analyses of this group are CHB and CPL (Tab. 1). The first three PCs explain 58% of the variance (27,20, and 11%, respectively). Ten PCs are needed to

account for 90% of the overall variance. The highest loadings on the 1 st PC are those of

characters LL, LF, and NC. This component is related with flower size and number of capitula. CALL, CLMLB and CALBE contribute most to the 2nd PC. These variables are related with

shape of ligulate florets and phyllaries. In the scatterplot of the specimens against the first two PCs, the three added species form

reasonably distinct clusters, although D. cavillieri only partially so (Fig. 5). The three

members of the central Asian group (D. altaicum, D. briquetii and D. falconeri (incl. D. turkestanicum)) form a single cluster. Therefore, ordination obtained with PCA already suggests that the three doubtful species are outliers. As expected, the discriminant analysis reinforces such outcome (results not shown).

Central Asian group

Characters excluded from the analyses of this group are CHB and CPL (Tab. 1). The first

three PCs explain 50% of the variance (24%, 15%, and 11%, respectively). Eleven PCs are

needed in order to explain 90% of the overall variance. The highest loadings on the 1st PC are

those of characters LL, LF, and DIAM. This component is related to the size of the flowers and

the capitula. Variables contributing the most to the 2nd PC are CLMLB, ABE, and NDA. This

component depicts the shape of the phyllaries and ligules. In the scatterplot against the first two PCs, no discrete clusters are shown, but the position of

D. altaicum is marginal and only slightly overlapped with other species (Fig. 6A).




cm 3 O

cl * A

2 A A* A

o^ a 0. stenoglossum 1 " D + A

o + a + + D. kamaonense

D-x-O

0' \m o ^ ? *

<x>+^" * 0. caw///e/7

? DD +* * * *

a + <^ a D. altaicum

-1 O D. briquetii *

^ * D. falconeri

+ D. falconeri

"D. turkestanicum" 1-,?-.-.-.-?

-3 -3-2-10 1 2

PC1 Fig. 5. Principal components analysis of the central Asian taxa in Doronicum (central Asian group +

D. stenoglossum, D. kamaonense, D. cavillieri). Scatterplot of the specimens against the first two principal

components axes.

Four variables remained in the discriminant analysis when the stepwise procedure was

followed (LF, LHCM, CAL and CLPLT). The first two canonical discriminant functions

account for 93% of the variance, the first one being correlated with LF and LHCM while the

second was with CAL. Classification results yielded 31 cases out of 40 (77%) assigned to the

correct group. Three of the 9 misclassifications involved confusions between

"?>. turkestanicum" and D. falconeri. Therefore, 85% of the specimens were classified into the

predetermined species when our taxonomy (Tab. 1) is considered. The scatterplot does not

provide a clear discrimination for the three species (Fig. 6B). Clear-cut clusters are not present, and the most distinct is that of D. briquetii. Specimens of D. falconeri labeled as

"D. turkestanicum" are adjacent, but not much overlapped with the remaining conspecific

samples. However, the structuring of the dots in the plot is consistent with the taxonomy of the

group.

DISCUSSION

Global matrix

A matrix containing data from 30 taxa is not likely to yield discrete clear-cut clusters

corresponding to taxonomic groups when analyzed with PCA. This is due to various reasons.

First, because PCA is not a clustering technique, but one that is designed to reduce data by

examining relationships among characters and producing a set of uncorrelated new variables.

Second, when 30 different biological entities are involved, it is expected that a significant

number of components of variation may occur in the data. Only a few of these components will

be represented in the scatterplots generated from the first PC axes. Characters that contribute

poorly to the main components of variation will thus be under-represented in the first PC axes.

Groups that are diagnosed on the basis of such characters will not be discriminated by

scatterplots of the first PCs. This situation applies particularly when the first three PC axes




3 al I A

0- o o

2 + ? ?o a o o

D * *

D * +

n' a o d D. altaicum 0 Q +

* *

dd D ?* O D.briquetii a ?

*+ +

+ + * * D. falconed -1 a + + D. falconeri

"D. turkestanicum"

-2 -3-2-1012

PC1

CN 3 u- B Q

2 a o ?

?o o +

1 v * O

^ D D + o *

0 o o + a+

"1 * + + + a D. altaicum

* ** O D.briquetii

* D. falconeri

-3 + D. falconeri * "O. turkestanicum"

A ^ - ^ 1

-4-20246

DF1 Fig. 6. Morphometric multivariate analysis of the central Asian group in Doronicum. A -

principal components analysis: scatterplot of the specimens against the first two principal components axes. B -

discriminant analysis: scatterplot of the specimens against the first two canonical discriminant functions.

together only explain half of the overall variance. Additionally, the characters that contribute the most to the first PC axes may be highly variable within species, a situation that also

produces a lack of clear-cut clusters. Part of the difficulties in obtaining clear-cut groups, and thus in testing the taxonomic usefulness of morphometric characters, can be overcome by reducing the number of taxa to be analyzed. As we remove species from the analysis, the number of components of the overall variance decreases, and thus the taxonomically-relevant characters, even if only for a given pair of species, are likely to move their influence onto the first PC axes. For this reason, reduced groups within Doronicum have been analyzed.




However, the fact that the first PC axis is primarily influenced by characters related to the

shape of the phyllaries - and not by, e.g., the size of vegetative organs

- is in principle a positive symptom about the ordination produced. Phyllaries are taxonomically-important characters not only in Doronicum but also in other Asteraceae (Bremer 1994). Therefore, the

trends detected in the scatterplot of the 291 specimens against the first two PCs are not

taxonomically meaningless. The fact that the samples belonging to the same group (e.g. D. plantagineum group, central Asian group) and species (e.g. D. stenoglossum) are plotted on

the same area of the multivariate space indicates that the taxonomic treatment is not

completely arbitrary. Not much more about taxonomic ordination, however, can be said on the

basis of such a large and complex data set.

Placement of species with uncertain affinities

The first purpose in analyzing the three reduced groups in this study was to examine the

position of several species of uncertain affinities with respect to the core members of

well-defined groups. In particular, we anticipated some clarification about the relative

affinities of D. columnae and D. carpaticum by analyzing them together with the core

representatives of the two putative closest groups {D. plantagineum and D. grandiflorum

groups). Under the same expectations, we examined the relative position of the Asian species D. cavillieri, D. kamaonense and D. stenoglossum, but compared them to a single group

(central Asian) because no other putative close groups were envisaged. The scatterplot of the specimens of the D. plantagineum group against the first two PCs

does not provide a conclusive discrimination for D. columnae and D. carpaticum (Fig. 2A).

Although confined in the upper left quadrant of the plot, the specimens from both species

appear intermingled with the rest. According to this result, these specimens cannot be

considered clear outliers with respect to the D. plantagineum s. str. group. It should be noted

that PCA is characterized by faithful representation of the distances between major groups of

clusters while distances between close neighbors may be distorted (Sneath & Sokal 1973). This is one of the reasons why ordination should be further checked with DA. Quite

surprisingly, the scatterplot of the first two canonical discriminant functions also fails to

separate D. columnae and D. carpaticum from the D. plantagineum s. str. group (Fig. 2B). This

is consistent with the fact that 7 of the 11 misclassified specimens involved confusions

between the D. plantagineum s. str. group and D. columnae or D. carpaticum. If patterns of

variation within the D. plantagineum s. str. group were markedly different to those in the two

species, we would expect the scatterplots against the first two canonical discriminant functions

to show a clear gap between the two species and the remaining members of the group. The fact

that no such gap is found, even though DA is a powerful technique for discrimination, suggests

that the two species are actually part or close relatives of the D. plantagineum s. str. group.

A comparison, therefore, is needed with their behavior in an analysis of the other closest

putative group. The inclusion of D. columnae and D. carpaticum in the analyses of the D. grandiflorum

group does not provide a conclusive answer to their taxonomic placement either. However,

when the results of this analysis are compared to those of the D. plantagineum group,

morphometric data suggest a closer affinity to the latter. Despite the fact that the PCA of the

D. grandiflorum group plus D. columnae and D. carpaticum does not reveal discrete clusters

(Fig. 4A), the two species {D. columnae in particular) are confined to the area with negative




values for the PCI. Unlike the situation in the other group, the discriminant analysis does

effectively separate these two species from D. grandiflorum, D. glaciale and D. clusii (Fig.

4B). The percentage of misclassified specimens (42%) is higher than in the analysis of the

D. plantagineum group. However, most confusions (20 out of 21) are due to problems of

identification either within the D. grandiflorum group (D. grandiflorum, D. glaciale and

D. clusii) or within the D. columnae + D. carpaticum pair. The fact that the second most likely classification for all the 50 specimens also remained within the same limits is a strong

argument for considering that D. columnae and D. carpaticum are outliers to the

D. grandiflorum group.

The closest relationship of the two species with the D. plantagineum s. str. group is

consistent with molecular data from the ITS sequences, but further evidence is needed since

the available sequence of a chloroplast marker (trnL-trnF) for D. columnae suggests otherwise

(Alvarez FernAndez et al. 2001). On morphological grounds, one of the synapomorphies of

the D. plantagineum s. str. group (the ciliate phyllaries) does not consistently appear in all

populations of D. columnae and D. carpaticum.

Besides the close relationships between D. columnae plus D. carpaticum and the

D. plantagineum s. str. group, a conclusion can be drawn from the analyses of the latter group.

This is the taxonomic affinities between D. columnae and D. carpaticum suggested on

morphological grounds (Alvarez FernAndez 1999). These two species largely or completely

overlap in the plots (Figs. 2A, 2B) and 4 of the 11 misclassifications involve confusion between them. Further, the second most-likely classification for 17 of the 20 specimens of both

species was the other one (i.e., D. carpaticum instead of D. columnae or vice versa).

The same strategy of adding taxonomically-uncertain species to reasonably-delimited

groups also gave positive results in the case of the three Asian species. The fact that the

specimens of D. kamaonense, D. stenoglossum and D. cavillieri form discrete clusters with

respect to the core of the central Asian group in the PCA scatterplot suggests that the three

species are outliers (Fig. 5). The situation of D. cavillieri is less clear than the situation of the

other two in this respect. The single cluster in which D. altaicum, D. briquetii and D. falconeri are integrated indicates that the group they form (central Asian) has morphometric support. Thus, the ordination obtained with the PCA is consistent with the taxonomic arrangement mainly based on qualitative morphological characters and on molecular data (Alvarez FernAndez 1999).

Species delimitation within cohesive groups

The second purpose in analyzing reduced groups was to explore whether morphometric characters could discriminate species forming seemingly natural assemblages within

Doronicum. Multivariate methods have been recently applied to similar problems in other

groups of Senecioneae (HodAlovA & Marhold 1996, 1998). As a whole, in our study the

results depended on the kind of analysis and to a lesser degree on the group. The PCA of the D. plantagineum s. str. group does not produce clear-cut clusters, but the marginal position of

D. hungaricum and D. orientale with respect to D. plantagineum is apparent, as is the

coincident behavior of specimens labeled "D. atlanticum" as compared to the remaining D. plantagineum (Fig. 3A). The discriminant analysis emphasizes the same pattern (Fig. 3B). Two conclusions follow. First, there is no clear morphometric support for the taxonomic

recognition of N African populations of D. plantagineum CD. atlanticum") against the



438 I. Alvarez Fernandez & G. Nleto Feliner

European populations. Still, the possibility of introgression from D. orientale in N African

populations of D. plantagineum exists (Alvarez Fernandez et al. 2001). The fact that the

second most likely classification for two of the ten N African specimens of D. plantagineum is

D. orientale leaves some room for this hypothesis. Unlike the morphometric analysis of the D. plantagineum s. str. group, the results of the

central Asian group {D. altaicum, D. briquetii, D. falconeri) do not provide a consistent

discrimination among species. However, even in the absence of clear-cut clusters, the

arrangement of the dots in the scatterplot from the DA seems to be a reflection of the taxonomy

(Fig. 6A, 6B). The placement of D. falconeri with respect to those conspecific populations

previously known as D. turkestanicum (adjacent but only partially overlapped) is consistent, but not conclusive in supporting our taxonomic criterion that they are synonyms. The

characters supporting a non-overlapping position of both species are primarily the length of

the disk and of the ray florets. We had recorded such partial differences, but consider that their

taxonomic relevance is at most doubtful. Inclusion of the binary variable HET improves discrimination between the heterocarpic D. falconeri (incl. D. turkestanicum) and the

homocarpic D. altaicum and D. briquetii. Multivariate techniques are quite robust to small

departures from normality (Marcus 1990, Legendre & Legendre 1998). Therefore,

including one or two qualitative characters in the framework of an exploratory analysis is

acceptable. However, since we are primarily interested in the potential utility of continuous

variables, it is preferable not to alter the selection conducted by the stepwise procedure in the

DA, which excluded HET from the analysis.

Between-species discrimination based on morphometric characters in the third group considered in this study {D. grandiflorum) was rather poor (results not shown). Neither PCA

nor DA produced discrete clusters corresponding to D. grandiflorum, D. glaciale and D. clusii.

This outcome is consistent with our taxonomic study based on morphological characters,

under a univariate approach, which failed to detect any differences between these species other

than the type of indumentum (Cavillier 1911, Alvarez Fernandez 1999). The inability of

morphometric techniques to separate the species of the D. grandiflorum group is also

consistent with molecular data, and not attributable to the properties of the multivariate

analyses.

In conclusion, the application of morphometric multivariate techniques to taxonomy in

Doronicum gave moderately satisfactory results. These are restricted to low taxonomic levels

and to groups containing a reasonably low number of species. On the whole, morphometric characters are a complementary source of information in groups where qualitative (in

particular, shared) characters are scarce, as is the case in Doronicum. This does not imply their

use in phylogenetic analysis, which poses serious problems (Chappill 1989, Stevens 1991,

Rae 1998, Thiele 1993). However, in the context of an exploratory analysis (Marcus 1990)

they can be very useful, by facilitating a scrutiny of patterns of variation and co-variation of

characters, and thus helping to make decisions regarding species recognition, taxonomic

status, as well as group limits or composition.

Acknowledgements: The authors are grateful to Javier Fuertes, Karol Marhold, Pablo Vargas as well as to two

anonymous reviewers for their constructive comments, which have substantially improved the manuscript, and

to Laura Barrios for assistance with statistical matters. This work has been supported by grant DGES

PB96-0849 of the Spanish Direccion General de Ensehanza Superior e Investigation Cientifica.




REFERENCES

ABBOTT L.A., BlSBY F.A., & ROGERS D.J. (1985): Taxonomic analysis in biology. Computers, models and

databases. Columbia University Press, New York.

ALVAREZ FERNANDEZ I. (1999): Sistemdtica del genero Doronicum L. (Asteraceae, Senecioneae) y andlisis

filogenetico basado en fuentes morfologicas y moleculares. Unpubl. PhD dissertation. Universidad

Complutense, Madrid.

ALVAREZ FERNANDEZ I. (2001): Four new combinations in Eurasian Doronicum L. (Asteraceae, Senecioneae). Novon 11:294-295.

ALVAREZ FERNANDEZ I. & NIETO FELINER G. (1999): Lectotypification of 16 species names in Doronicum

(Asteraceae, Senecioneae). Taxon 48: 801-806.

ALVAREZ FERNANDEZ I. & NlETO FELINER G. (2000): A new species of Doronicum (Asteraceae, Senecioneae) from central China. Ann. Bot. Fenn. 37: 249-253.

Alvarez Fernandez I., Fuertes Aguilar J., Panero J.L. & Nieto Feliner G. (2001): A phylogenetic

analysis of Doronicum (Asteraceae, Senecioneae) based on morphological, nuclear ribosomal (ITS) and

chloroplast (trnL-F) evidence. Molec. Phyl. Evol. 20: 41-64.

AVETISJAN V.E. (1980): Rod Doronicum L. v Armenii (The genus Doronicum in Armenia). Biol. Zhurn.

Armenii 33: 532-534.

BREMER K. (1994): Asteraceae. Cladistics & classification. Timber Press, Portland, Oregon. CAVILLIER F. (1907): Etude sur les Doronicum a fruits homomorphes. Annuaire Conserv. Jard. Bot. Geneve

10: 177-251.

CAVILLIER F. (1911): Nouvelles etudes sur le genre Doronicum. Annuaire Conserv. Jard. Bot. Geneve 13-14:

195-368.

CHAC6N R. (1987): Contribucion al estudio taxonomico del genero Doronicum L. (Compositae) en la

Peninsula Iberica. Anales Jard. Bot. Madrid 43: 253-270.

CHAPPILL J.A. (1989): Quantitative characters in phylogenetic analysis. Cladistics 5: 217-234.

DE PINNA M.C.C. (1991): Concepts and tests of homology in the cladistic paradigm. Cladistics 7: 367-394.

DUVIGNEAUD J. (1992): Le genre Doronicum L. en Belgique et dans les regions voisines. Nat. Mosana 45:

81-92.

EDMONDSON J.R. (1973): Notes on Doronicum L. in SW Asia. Notes Roy. Bot. Gard. Edinburgh 32:255-258.

EDMONDSON J.R. (1975): Doronicum L. In: DAVIS P. H. (ed.), Flora of Turkey and the East Aegean Islands 5,

Edinburgh University Press, Edinburgh, pp. 137-145.

EDMONDSON J.R. (1978): The genus Doronicum L. in Iran. Notes Roy. Bot. Gard. Edinburgh 37: 67-73.

HODALOVA I. & MARHOLD K. (1996): Sympatric populations of Senecio ovatus subsp. ovatus, S. germanicus

subsp. germanicus (Compositae) and their hybrid in the Carpatians and the adjacent part of Pannonia. Flora

191:283-290.

HODALOVA I. & MARHOLD K. (1998): Morphometric comparison of Senecio germanicus and S. nemorensis

(Compositae) with a new species from Romania. Bot. J. Linn. Soc. 128: 277-290.

HOLLIS S. & BRUMMITT R.K. (1992): World geographical scheme for recording plant distributions. Carnegie Mellon University, Pittsburgh.

KLECKA W.R. (1980). Discriminant analysis. Quantitative applications in the social sciences. Sage University paper no. 19. Newbury Park.

LEGENDRE P. & LEGENDRE L. (1998): Numerical ecology. Elsevier, Amsterdam.

MARCUS L.F. (1990): Traditional morphometries. In: ROHLF F.J. & BOOKSTEIN F.L. (eds.), Proceedings of the

Michigan Morphometries Workshop, University of Michigan, Ann Arbor, pp. 77-122.

PATTERSON C. (1988): Homology in classical and molecular biology. Molec. Biol. Evol. 5: 603-625.

P?REZ MORALES C. & PENAS A. (1990): Sobre algunos Doronicum ibericos. Lagascalia 15: 151-160.

P?REZ MORALES C, PENAS A., LLAMAS F. & ACEDO C. (1994): Doronicum pubescens sp. nov. Lazaroa 14:

5-12.

RAE T.C. (1998): The logical basis for the use of continuous characters in phylogenetic systematics. Cladistics

14:221-228.

SNEATH P.H.A. & SOKAL R.R. (1973): Numerical taxonomy. The principles and practice of numerical

classification. W. H. Freeman & Co., San Francisco.




STEVENS P.F. (1991): Character states, morphological variation and phylogenetic analysis: a review. Syst. Bot.

16: 553-583.

THIELE K. (1993): The Holy grail of the perfect character: the cladistic treatment of morphometric data.

Cladistics 9: 275-304.

WlDDER F.J. (1925): Eine neue Pflanze der Ostalpen -Doronicum (Subsectio Macrophylla) cataractarum -

und ihre Verwandten. Repert. Spec. Nov. Regni Veg. 22: 113-184.

Received 10 July 2000, revision received and accepted 16 March 2001

Encl. Appendix pp. 441-444



Morphometric characters In Doronicum 441

APPENDIX 1

List of the specimens used in the multivariate study. Main geographic subdivisions follow HOLLIS &

BRUMMITT(1992).

Doronicum cavillieri Alvarez Fernandez et Nieto Fel.

China (south-central): T'ao river basin (VI. 1925 J.F. ROCK BM); ibidem (VI. 1925 J.F. ROCK 12389 NY); ibidem (VI. 1925 J.F. ROCKE); ibidem (VI. 1925 J.F. ROCK 12192 NY); Tebbu country (1925 J.F. ROCKGH); ibidem (1925 J.F. ROCK K); ibidem (1925 J.F. ROCKNY); ibidem (1925 J.F. ROCK W).

Doronicum kamaonense (DC.) Alvarez Fernandez Nepal: Balangra pass (28.VII. 1952 O. POLUNIN et al. E); Ghurchi Lagua (22.VI. 1952 O. POLUNIN et al. G).

Jammu-Kashmir: Gurais (6.IX.1892 J.F. DUTHIE BM); Khelanmarg (2.VIII.1956 O. POLUNIN B); ibidem

(2.VIII.1956 O. POLUNIN BM); Rampur (5.VII.1940 F. LUDLOW & G. SHERRIFF BM); Sinthan pass (10.VIII.1943 F. LUDLOW & G. SHERRIFF E). Pakistan: Hazara district (VI.1955 G.L. WEBSTER & J. Sack G).

Doronicum oblongifolium DC.

Turkey: Artvin, Yalnizcam Silsilesi (10.VII.1967 ALBURY et al. K); Coruh, Kordevan dag (28.VI.1957 P.H. DAVIS & I.G. HEDGE K); ibidem (28.VI.1957 P.H. DAVIS & I.G. HEDGE W). North Caucasus:

Daghestan (without date G.F.R. RADDE G); Zagedan (7.VII. 1989 A. DOLMATOVA et al. LE). Transcaucasus:

Aragac (13. VII. 1975 E. GABRIELIAN E); ibidem (13.VII.1975 E. GABRIELIAN G; 4. VI. 1988 K. TAMANJAN G); Armenia (without collector and date E); Carthalinia (VI. 1881 A.H. BROTHERUS & V.F. BROTHERUS 501G).

Doronicum pardalianches L.

Belgium: Esneux (28.V.1976 J. DUVIGNEAUD B). France: Loire (20.V.1894 H.E. JEANPERT B); Macou

(without date and collector B). Germany: Brimav (21.V.1894 FERGES B); Mark Branderburg (19.V.1974 H. SHOLZ B). Great Britain: Stainton-in-Peak (18.VI.1862 J. BALL MA 171821). Italy: San Valmazzo

(14.V.1934 BASCHANT B). Spain: Barcelona, Valvidriera (without date and collector MA 129791); Huesca, sierra de Guara (24. VI. 19951. ALVAREZ et al. MA); Lerida, sierra del Cadi (29.VI. 19961. ALVAREZ et al. MA).

Doronicum stenoglossum Maxim.

China (north-central): Ganzu, T'ao river basin (VII. 1925 J.F. ROCK GH); Tebbu country (VIII. 1926 J.F. ROCK E); ibidem (VIII.1926 J.F. ROCK NY). China (Tibet-Qinghai): Dari-Xian (14.VIII.1993 T.N. HO et al.

MO); Reting (28.VII.1942 F. LUDLOW & G. SHERRIFF BM). China (south-central): Lichiang range (VIII. 1906 G. FORREST BM); Likiang, Tungshan (V. 1923 J.F. ROCK GH); west Yunnan (1930 G. FORREST E);

Yunnan (without date T.T. Yu GH); Yunnan, Muli (21.X.1937 T.T. Yt) E).

Central Asian group

Doronicum altaicum Pall. Russia (Siberia): Altay (VII. 1947 A. KUMrNOVA & PAVLOVA GH); ibidem (without date PALLAS BM);

ibidem (14.VIII.1923 V. SAPOSHNIKOV W); ibidem (without date and collector E); Sayan (1.VII.1964 E. PENKOVSKAYA & I. KRASNOBOROV LE); Tomsk, Kara-Kokshi (21.VII.1915 P.N. KRYLOV LE); Tuva

(12.VII.1970 I. KRASNOBOROV LE); ibidem (2.VIII.1975 M. LOMONOSOVA & D. SHAULO LE); ibidem (3.VII.1971 S.N. VIDRINA LE); Siberia (30.VII.1902 V.I. KOMAROV LE).

Doronicum briquetii Cavill. China (south-central): Dokerla (VIII. 1935 C.W. WANG GH); Hung-po (VI. 1932 J.F. ROCK GH); ibidem

(VI. 1932 J.F. ROCK K); Konka mount (VIII. 1928 J.F. ROCK GH); Mekong on Kaakerpo (1932 J.F. ROCK GH); Peimashan (VII. 1923 J.F. ROCK K); Wuli-la (1932 J.F. ROCK GH). China (Tibet-Qinghai): Kongbo (21.VI.1947 F. LUDLOW et al. BM); ibidem (21.VI.1947 F. LUDLOW et al. G); ibidem (16.VIII.1947 F.

LUDLOW et al. BM).

Doronicum falconeri C.B. Clarke India: Dhaola Dhar (7.VII.1939 G. SHERRIFF BM); ibidem (7.VII.1939 G. SHERRIFF 7405, sheet 2 BM);

Rotang (11.VII.1941 N.L. BOR E); Shonthar Gali (2.VIII.1935 F. LUDLOW & G. SHERRIFF E). Jammu-Kashmir: Baltistan (22. VIII. 1936 W. KOELZ GH); ibidem (3 .VIII. 1940 R.R. STEWART NY); Bringhi




(23.VIII. 1943 F. LUDLOW & G. SHERRIFF BM); Gittidas (15.VII.1953 F. SCHMID G); Haramukh (29.VII.1940 F. LUDLOW & G. SHERRIFF BM); Kero Lugma glacier (24.VII. 1939 RUSSELL BM). China (Xinjiang):

Bagadushung (14.VI.1879 A. REGEL E*); Turkestania, Bogdo-ola (VIII. 1908 G. MERZBACHER W*). Kazakhstan: Alatau, Lepsa (1841 G.S. KARELIN & LP. KlRILOV BM*); Katon-Karagaj (10.VIII.1930 P.A.

SMrRNOV W*); Ketmenj (1.VII.1964 I. ROLDUGIN G*); ibidem (1.VII.1964 I. ROLDUGIN MA 358613*). Kirgizistan: Kungei Alatau (17.VII.1896 V.F. BROTHERUS G*); Terskei Alatau (without date and collector

GH*); Vernenskij (without date N.D. SOKALSKIJ E*). Russia (Siberia): Altay, Kurkure (21.VII. 1977 MARIN

LE*). * Labeled as D. turkestanicum CAVILL. in the analyses (see Material and methods)

Doronicum austriacum group

Doronicum austriacum Jacq.

Andorra: Pirineos (VII. 1949 LOSA & MONTSERRAT MA 155589). Austria: Styria inferior (1842 R.C.

ALEXANDER E). Bulgaria: Sitovo (VIII. 1896 V. STRIBRNY B). Italy: monte Nevon (30.VI. 1935 V.

ENGELHARDT B). France: Cerdagne Carlit (31.VII.1916 F. SENNEN MA 129784). Germany: Heilbrunn

(VI. 1890 J. JAHN B). Greece: Kastoria (1965 O. POLUNIN E); Kerkini, mt. Belles (4.VII.1981 A. STRID et al.

B); Pella, Kaimaktsalan (13.VIII.1977 W. GREUTER G). Yugoslavia: Bitola (22.VII.1970 J.R. EDMONDSON

E).

Doronicum carpetanum Boiss. et Reut. ex Willk. subsp. carpetanum

Spain: Avila, Hoyos del Espino (28.VI.1987 G6MEZ MANZANEQUE et al. MA); Burgos, pico Mancillas

(14.VII.1984 BENEDI et al. MA 334336); Logrono, Canales de la Sierra (6.VII.1995 I. ALVAREZ et al. MA);

Ezcaray (20.VII.1991. PEREZ et al. MA 560311); Lugo, Tres Obispos (27.VII.1986 G. NlETO FELINER & J.

PEDROL MA 502993); Madrid, Penalara (VIII. 1911 F. BELTRAN MA 129727); ibidem (7.VII.1986 M. LUCENO & P. VARGAS MA 448157); Salamanca sierra de Candelario (21.VI. 1986 LANSAC & G. NlETO

FELINER MA 421399); Soria, Santa Ines (27.VII.1972 A. SEGURA ZUBIZARRETA MA 360095).

Doronicum carpetanum subsp. diazii (Perez Morales et Penas) Alvarez Fernandez

Spain: Leon, Abelgas (27.VII.1988 E. PUENTE & C. PEREZ MORALES MA 489306); ibidem (27.VII.1988 E. PUENTE & C. PEREZ MORALES MA 502699); Leon, Cornin (without date and collector E); Soria, sierra de

Urbion (10.VII.1935 L. CEBALLOS & C. VlCIOSO MA 129726); ibidem (10.VII.1935 L. CEBALLOS & C.

VlCIOSO MA 129739); ibidem (11.VI.1978 P. HARROLD & R.J.D. McBEATH E); ibidem (VII.1958 N.Y.

SANDWITH K); ibidem (VII.1958 N.Y. SANDWITH, sheet 2 K).

Doronicum carpetanum subsp. kuepferi(R. Chacon) Alvarez Fernandez

Spain: Avila, sierra de Gredos (without date and collector MA 445748); Caceres, sierra de Majarreina

(7.VIII.1946 S. RIVAS GODAY MA 155587); ibidem (7.VIII.1946 S. RlVAS GODAY MA 348763); Salamanca, Calvitero (26.VII. 1989 S. RlVAS MARTINEZ et al. MA 538496); ibidem (30.VI. 1985 R. VOGT B); Salamanca,

Candelario, (18.VII.1980 E. VALDES BERMEJO etal. MA 445798); ibidem (18.VII.1980 E. VALDES BERMEJO

et al. MA 445798a); ibidem (18.VII.1980 E. VALDES BERMEJO et al. MA 445798b); Salamanca, El Trampal

(10.VII.1989 G. NIETO FELINER et al. MA 472502); Salamanca, sierra de Bejar (28.VII.1982 F. NAVARRO &

C.J. VALLE MA 286039).

Doronicum carpetanum subsp. pubescens (Perez Morales, Penas, Llamas et Acedo)

Aizpuru

Portugal: serra da Estrela (19.VII.1997. I. ALVAREZ et al. MA). Spain: Asturias, lagos de Saliencia

(26.VII. 1988 M. LUCENO & P. VARGAS MA 449967); Cantabria, monte Gulatrapa, (2. VII. 1983 C. AEDO MA);

Cantabria (27.V.1990 S. PATINO et al. MA 537973); Coruna, Caaveiro, (25.IV.1981 F. AMICH et al. MA

311144); Coruna, Puente Carreiras (29.V. 1953 F. BELLOTMA 504155); Leon, circo Cebollero (16.VII.1974 B.

CASASECA & F.J. FERNANDEZ DlEZ MA 197037); ibidem (16.VII.1974 B. CASASECA & F.J. FERNANDEZ DIEZ MA 345401); Leon, Posada de Valdeon, (14.VII.1978 A. CHARPIN B); Palencia, pto. de Piedrasluengas

(14.VII.1995 I. ALVAREZ et al. 919/4 MA); ibidem (14.VII.1995 I. ALVAREZ et al. 919/10 MA).

Doronicum cataractarum Widder

Austria: Koralpe (3.VIII.1935 B. FEST B); ibidem (without date LEMPERG K); ibidem (16.VII.1947 F.J.

WIDDER GZU); ibidem (9.IX.1925 F.J. WIDDER B); ibidem (1.VIII. 1926 F.J. WIDDER K); Seebach

(28.VIIL1939. F.J. WIDDER B); ibidem (24.VIII.1936 F.J. WIDDER G).




Doronicum corsicum (Loisel.) PoiR.

France (Corsica): Aitone (1885 E. REVERCHON B); ibidem (1885 E. REVERCHON E); ibidem (1885 E. REVERCHON, sheet 2 E); ibidem (1885 E. REVERCHON NY); Fiumorbo (28.VII.1849 KRALIK E); Guagno (VIII.1847 REQUIEZ B); Incudine (2.VIII.1986 J. LAMBINON MA 367224); Mangamullo (18.VII.1906 H.

GYSPERGER B); Tavignano (13.VIII.1849 KRALIK E); Vizzabona (without date and collector B).

D. grandiflorum group

Doronicum clusii (All.) Tausch Austria: Ferwallgruppe (2.VIII.1942 W. FREIBERG MA 358526); Stilfser Joch (10.VIII.1911 M.

SCHREIBER MA 129736). Slovakia: Vysoke Tatry (6.VIII.1933 J. DOSTAL MA 411781); ibidem (24.VII.1893 L. GIRAUDIAS MA 129718); ibidem (26.VI.1915 J.B. KUMMERLE & G. TIMK6 B); ibidem (8.VII.1918 K. RONNIGER G). Italy: Bormio, passo dello Stelvio (4.VIII.1997 I. ALVAREZ et al. MA); Trento, coll del Cue

(3.VIII.1997 I. ALVAREZ et al. MA). Poland: Zakopane (20.VI.1961 W. HEMPEL B). Switzerland: Bernina

(18.VII.1990 S. CASTROVIEJO et al. MA 484983).

Doronicum glaciate (Wulfen) Nyman Austria: Hochechwabgebirge (5.VIII. 1887 H. STEININGER B); Hochplateau (VI. 1906 J. BORNMULLER B);

Maushen (18.VII.1907 V. ENGELHARDT B); Menspitze (19.VII.1988 F. JACQUEMOUD G); Raxalpe (27. VI. 1906 J. BORNMULLER B); Weissenbach (30.VI. 1900 G. TREFFER G); ibidem (30.VI. 1900 G. TREFFER, sheet 2 G). Germany: Hasenthal Prettan (VIII. 1882 G. TREFFER B). Italy: Trento, coll Rodella (2.VIII. 19971.

ALVAREZ et al. MA); Groden (18.VII.1907 J. BORNMULLER B).

Doronicum grandiflorum Lam. Austria: Bondone (8.VII.1899 S. ClMAROLLI G). France: Ariege (27.VII.1982 A. CHARPIN & M.

DITTRICH G); Galibier (3.VIII.1858 C. OZANON G); Pyrenees, vallee d'Ossoue (2.VIII.1996 A. HERRERO

MA). Italy: Belluno (11 .VII. 1970 F. DUSA & G. MORTIN MA 360098); Cuneo (4.VIII. 1982 A. CHARPIN & R. SALAMAN G); Tuscone di Lumpelli (5.VIII. 1912 P. CHENEVARD G). Spain: Huesca, pico Aneto (26.VII. 1997 T. ALMARAZ MA); Leon, Pena Prieta (14.VII. 1990 M.L. GIL ZOftlGA & J.A. ALEJANDRE MA 532701); Leon, Pena Ubina (8.VII.1990 C. AEDO MA).

D. plantagineum group

Doronicum carpaticum (Griseb. et Schenk) Nyman Hungary: without locality (VII. 1917 ADAMOVIC K). Romania: Bulea (23.VII.1914 J. TUZSON B);

Ceahlau (11.VII. 1922 I. GRINTESCU G); Transsilvania (without date SCHUR B); Vertop (20.IV. 1873 L.P. SIMKOVICS B); Vertop et Vertopul (without date L. SlMONKAI B); ibidem (without date L. SlMONKAI G); Zernest (30.VI.1900 WALZ MA 129725). Ukraine: Bliznitza mts. (28.VI.1950 K.N. IGOSHINA MO); Chornogora (16.VII.1938 G. KOZIJ MO).

Doronicum columnae Ten.

Austria: Praxersee (without date A. KERNER E). Bulgaria: Salzica (16.VI.1974 M. MARKOVA et al. E). Greece: Parnassi (24.VII.1854 T.G. ORPHANIDES G); Sterea Ellas (27.VI.1982 I. HAGEMANN et al. B); Thessalischer Olymp. (VII. 1960 F. SORGER B); Trapeza (11 .VI. 1937 E.K. BALLS & W.B. GOURLAY E). Italy: Corniolo (28.V.1976 F.L. CHIAPELLA & L. POLDINI MA) 358528; Groden (18.VII.1907 J. BORNMULLER B). Romania: Schuler (30.V.1886 ROMER B). Yugoslavia: Frebovic (V.1888 BECK & FlALA G).

Doronicum hungaricum Rchb. f.

Austria: Wolfsthal (10.V.1889 W. STEINITZ E). Hungary: Budam (without date J. KOVATS E); Farkasvolgy (without date FlLARSZKY & SCHILBERSZKY BM); ibidem (FlLARSZKY & SCHILBERSZKY E); Solymos (11.V.1867 M. VRABELYI E). Romania: Ia?i (7.VI.1967 M. TOMA BM); Vlasca (V.1934 P.

CRETZOIU B); Yugoslavia: Kis (without date JLIE B); Tapeider (1888 J. BORNMULLER B). Doronicum orientale Hoffm.

Austria: Theresienthale (10.VI.1895 E. KHEK B). Greece: Mitilinis (27.IV. 1987 A. STRID et al. G). Italy: Potenza (12.V.1933 O. GAVIOLI MA 129723); Vico del Gargano (16.IV.1976 M. NYDEGGER G). Turkey: Antalya (28.IV. 1959 E. HENNIPMAN et al. B); Byzantii in silva Belgradensi (7.V.1899 J. BORNMULLER B);




Istanbul, Bahcekoy (8.IV.1959 E. HENNIPMAN et al. B); Zekeriekeny (12.IV. 1904 G.V. AZNAVOUR B).

Yugoslavia: Hudowa (10.IV.1918 J. BORNMULLER B); Rakovica (IV. 1887 S. PETROVIC G).

Doronicum plantagineum L.

France: Haute-Mame, Louze (6.V.1991 B. RETZ MA 532469); Verrieres-le-Buisson (12.V.1973 B. RETZ MA 358614). Great Britain: Great Saling, Essex (20.V.1886 H.E. FOX B). Portugal: Estremadura, Malveira

(29.IV.1976 B. RAINHA MA 129715). Spain: Cadiz, Grazalema (21.IV.1982 G. LOPEZ & R. MORALES MA

443484); Cuenca, Talayuelas (V. 1980 G. MATEO MA 442886); Leon, Soto de Sajambre (4.V. 1967 H. SCHOLZ & P. HIEPKO B); Madrid, sierra de Guadarrama (V.1912 C. VlCIOSO MA 129704); Salamanca, Linares de Riofrio (17.V.1968 B. CASASECA MA 191689); Zaragoza, sierra de Vicort (22.IV. 1908 C. VlCIOSO MA

129694). Algeria: Kabylie (VI. 1898 E. REVERCHON BM**); ibidem (VI. 1898 E. REVERCHON G**); Tala

Guilef (19.VI.1975 P.H. DAVIS BM**); ibidem (19.VI.1975 P.H. DAVIS E**); Teniet El Had (2.V.1937 A.H.G. ALSTON & N.D. SIMPSON BM**); ibidem (31.V.1975 P.H. DAVIS E**). Morocco: Ain Leuh

(21.V.1924 E. JAHANDIEZ MA 129782**); Dai et Achlet (4.VI. 1923 E. JAHANDIEZ BM**); Ifrane (6.VI.1971 G. BOCQUETBM**).

** Labeled as D. atlanticum CHABERT in the analyses (see Material and methods).

South-west Asian group

Doronicum cacaliifolium Boiss. et Heldr.

Turkey: Isauria, Geyik dag (28.VIII. 1947 P.H. DAVIS E); ibidem (28.VIII.1947 P.H. DAVIS G); ibidem

(28.VIII. 1947 P.H. DAVIS, sheet 1 K); ibidem (28.VIII. 1947 P.H. DAVIS, sheet 2 K); ibidem (28.VIII. 1947 P.H.

DAVIS W).

Doronicum do/ichotrichum Cavill. Iran: Dimelo (4.VI. 1956 F. SCHMID G); Maku (22.VI. 1974 SlAMI W); Azerbaydzhan, Kalibar (26.VI. 1978

TERMEH et al. G). Iraq: Helgord range (3.IX.1957 A. RAWI & I. SERHANG K). Turkey: Artvin,

Yalnizcam-Gebirge (4.VIII.1981 RAUS B); Coruh, Kordevan dag (29.VI. 1957 P.H. DAVIS & I.G. HEDGE E);

Kars, Yagmurlu dag (13.VI. 1957 P.H. DAVIS & I.G. HEDGE BM). Transcaucasus: Ossetia, Didi Liachva

(22.VII.1881 A.H. BROTHERUS & V.F. BROTHERUS K); Ermani (4.VI.1956 F. SCHMID W).

Doronicum haussknechtii Cavill.

Turkey: Berytdag (5.VIII.1865 H.K. HAUSSKNECHT W); Giresun, Karagol (5.VIII.1965 C. TOBEY E);

Kayseri, Isikdagi (21.VII. 1992 H. DUMAN & Z. AYTAR GAZI); Maras, Binboga dag(15.VII. 1952 P.H. DAVIS

et al. E).

Doronicum macrophyllum Fisch. subsp. macrophyllum Iran: Qareh Dagh (20.VII.1971 J. LAMOND & F. TERMEH K). North Caucasus: Checheno-Ingushiya

(9. VII. 1988 D. GELTMAN et al. LE); Kavardino-Balkariya (18.VII.1990 MENITSKIJ et al. LE). Transcaucasus:

Abkhaziya (20.VIII.1990 DOLMATOVA et al. LE); Anneniya (without date and collector W); Azerbaydzhan, Kuba (8.VII.1935 KARJAGIN NY); Georgia (1838 R.F. HOHENACKER K); Allahverdi (without collector and

date BRNM); Tiflis (without date and collector MO). Turkey: Rize, Izikdere (21.VII. 1984 A. GONER & M.

VURAL GAZI); Trabzon, Bayburt (11.VII. 1960 J.D.A. STAINTON & HENDERSON K).

Doronicum macrophyllum subsp. sparsipilosum (J.R. Edm.) Alvarez Fernandez

Turkey: Bolu, Ala dag(12.VII. 1962 P.H. DAVIS & COODE E); ibidem (12.VII.1962 P.H. DAVIS & COODE

K); Kastamonu, Ilgaz Daglari (27.VI.1971 J.R. EDMONDSON E); ibidem (27.VI.1971 J.R. EDMONDSON, sheet

2 E); ibidem (28.VII.1962 P.H. Davis et al. E); ibidem (5.VII.1984 M. NYDEGGER G).

Doronicum maximum Boiss. et A. Huet

Turkey: Erzurum, Karliova-^at (21.VII. 1982 M. NYDEGGER G); Giresun, Balabandaglari (7.VIII.1952 P.H. DAVIS et al. BM); ibidem (7.VIII.1952 P.H. DAVIS et al. E); ibidem (7.VIII.1952 P.H. DAVIS et al. K).

Doronicum reticulatum Boiss.

Turkey: Bolu, Ala dag (17.VII.1967 ALPAY E); ibidem (12.VII.1962 P.H. DAVIS & COODE E); ibidem

(12. VII. 1962 P.H. DAVIS & COODE, sheet 2 E); ibidem (12.VII. 1962 P.H. DAVIS & COODE K); Bursa, Uludag,

(24.VII.1993 Z. AYTAC & M. EKICI GAZI); ibidem (9.VII.1978 BERNARDI G); Phrygia, Wilajet Konia

(9.VIL1899 J. BORNMULLER B).



a multivariate approach to assess the taxonomic utility of morphometric characters in doronicum...

Documents