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Tillandsia capillaris Ruiz & Pav., which belongs to the subgenus Diaphoranthema is distributed in Ecuador, Peru, Bolivia, northern and central Argentina, and Chile, and includes forms that are difficult to circumscribe, thus considered to form a complex. The entities of this complex are predominantly small-sized epiphytes, adapted to xeric environments. The most widely used classification defines 5 forms for this complex based on few morphological reproductive traits: Tillandsia capillaris Ruiz & Pav. f. capillaris, Tillandsia capillaris f. incana (Mez) L.B. Sm., Tillandsia capillaris f. cordobensis (Hieron.) L.B. Sm., Tillandsia capillaris f. hieronymi (Mez) L.B. Sm. and Tillandsia capillaris f. virescens (Ruiz & Pav.) L.B. Sm. In this study, 35 floral and vegetative characters were analyzed with a multivariate approach in order to assess and discuss different proposals for classification of the Tillandsia capillaris complex, which presents morphotypes that co-occur in central and northern Argentina. To accomplish this, data of quantitative and categorical morphological characters of flowers and leaves were collected from herbarium specimens and field collections and were analyzed with statistical multivariate techniques. The results suggest that the last classification for the complex seems more comprehensive and three taxa were delimited: Tillandsia capillaris (=Tillandsia capillaris f. incana-hieronymi), Tillandsia virescens s. str. (=Tillandsia capillaris f. cordobensis) and Tillandsia virescens s. l. (=Tillandsia capillaris f. virescens). While Tillandsia capillaris and Tillandsia virescens s. str. co-occur, Tillandsia virescens s. l. is restricted to altitudes above 2000 m in Argentina. Characters previously used for taxa delimitation showed continuous variation and therefore were not useful. New diagnostic characters are proposed and a key is provided for delimiting these three taxa within the complex.
Tillandsia capillaris, Bromeliaceae, species complex, morphometry, distribution
The subfamily Tillandsioideae comprises 10 genera (
Tillandsia capillaris s. l. is distributed from southern Ecuador to central Argentina and Chile, between altitudes from 300 m to 4000 m. (
In the dry forests of central Argentina (called Bosque Serrano,
The Tillandsia capillaris complex constitutes a group of related taxa with a gradual morphological variation. The nomenclatural history itself reflects the complex nature of Tillandsia capillaris and allies. The available classifications (
In the past two centuries several species that are currently included in the Tillandsia capillaris complex were described.
The currently accepted classification in Argentina (
The lastest revision of the subgenus Diaphoranthema in South America was done by
In this contribution we analyzed the morphological variation of Tillandsia capillaris taking as the starting point the five forms defined by
Herbarium specimens from CORD and LIL (
Qualitative and quantitative characters used for the morphometric study of the complex Tillandsia capillaris.
Quantitative characters | Qualitative characters |
---|---|
Continuous variables | Binary variables |
1-Length of fertile shoot (mm). | 5-Type of stem (simple, ramified: 0; 1). |
2-Length of stem (mm). | 7-Leaf blade apex (rounded, apiculate: 0; 1). |
3-Length of leaf blade (mm). | 8-Arrangement of the leaf (appressed, non appressed: 0; 1). |
4- (half) Width of leaf blade (mm). | 10-Leaf sheath exposure (visible, covered by the lower contiguous sheaths: 0; 1). |
15-Length of scape (mm). | 12-Type of peltate hairs |
18- (half) Width of bract (mm). | 16-Scape position (axillary, terminal: 0; 1). |
19-Length of floral bract (mm). | 20-Floral bract shape (round and wide, triangular and elongated: 0; 1). |
25-Length of the sepals (mm). | 21-Floral bract apex (acute, mucronate: 0; 1). |
30-Length of fruit (mm). | 26-Sepal dimension (exceeding the bract, equaling the bract: 0; 1). |
31- (half) Width of fruit (mm). | 29-Sepal shape: (ovate-lanceolate, acute: 0; 1) |
34-Length of seed (mm). | 32-Endocarp shape (shaped, not shaped: 0; 1). |
35-Length of embryo (mm). | |
Discontinuous (or discrete) variables | Multistate variables |
6-Number of branches (n°). | 9-Type of leaf blade (straight, half-curved, curved: 0; 1; 2). |
11-Number of leaves per linear cm of shoot (nº). | 13-Winged trichomes position in the leaf (only in the base, in the base and in the middle part, in the whole leaf: 0; 1; 2). |
17-Number of inflorescences per branch (n°). | 14-Pilosity of the leaf (low, medium, high: 0; 1; 2). |
22-Number of nerves in the floral bract (n°). | 24-Floral bract indument (glabrous, half pubescent, pubescent: 0; 1; 2). |
23-Number of nerves joined together at the apex of bracts (n°). | 33-Exocarp shape (straight, curved, very curved: 0; 1; 2). |
27-Association degree of the adaxial sepals (%). | |
28-Association degree of the abaxial sepals (%). |
1Types of trichomes: 1-radially symmetric, 2-one developed wing, 3-two wings developed
Non-parametric Kruskal-Wallis tests (KW) were run for all the variables among the taxa considered. Box-plots were made for continuous variables.
A two-steps analysis was carried out to detect the most informative characters. First, a Principal Component Analysis (PCA) was run using all characters (
Results of character comparisons showed significant differences (Fig. 1; except for “number of branches” – KW test; H=4.68; P= 0.24) among the putative taxa but with unclear trends (Fig. 1). For example, Tillandsia capillaris f. virescens showed significantly lower values compared to the other taxa for several traits (length of: fertile shoot, leaf blade, scape, fruit, seed and of embryo; Figs 1a, c, d, g, h, i respectively). Tillandsia capillaris f. cordobensis differed from all the other forms by the longer size of leaves, of floral bracts, of sepals, the lower number of leaves per linear cm of shoot and the highest number of nerves joined together at the apex of bracts (Figs 1c, e, f, j, k, respectively). Tillandsia capillaris f. hieronymi showed significant differences with an intermediate size of the fertile shoot, the scapes, and lower number of nerves joined together at the apex of bracts (Figs 1a, d, k). Tillandsia capillaris f. capillaris and Tillandsia capillaris f. incana did not show significant differences and these forms are overlapped with the other forms considering this set of characters (Figs 1a–l).
In the PCA, the first three components explained 50.5 % of variability (25.9, 16.5, and 8.1 % respectively) (results not shown). Analyzing the variables individually, only 19 variables were selected to explain the variance among taxa (see material and methods), considering the ones which showed values up to 0.20 (Table 2). A second PCA using these 19 characters showed that the principal two axes provide a clear ordination of the OTUs into separate groups (Figure 2). The two principal axes together account for 64.4% of the variability. The variance of the first component included quantitative variables (lengths of leaf blade, bract, and sepals, number of leaves per linear cm of shoot, and fusion degree of the adaxial sepals), and qualitative variables (arrangement of the leaf, sepal dimension, type of leaf blade, floral bract shape, sepal shape, indument of the floral bract and leaf sheath exposure). The variance of the second component was supported by quantitative variables concerning the vegetative and the inflorescence size (lengths of fertile shoot, stem, scape, fruit, seed, embryo, and width of bract; Table 2). Figure 2 shows the grouping tendency among the OTUs for this set of 19 variables.
Title: Principal components analysis results for the Tillandsia capillaris complex. Legend: PCA results for 5 taxa of the complex Tillandsia capillaris using 35 quantitative and qualitative traits (see M&M for details). The percentages of variance for the two principal components were obtained in the PCA analysis from all the characters. * indicates the values >0.20
Principal components | ||
Character | Axis 1 | Axis 2 |
---|---|---|
Length of fertile shoot (LgFS) | 0.06 | 0.36* |
Length of stem (LgSt) | 3.8E-03 | 0.22* |
Length of leaf blade (LgLB) | 0.25* | 0.12 |
Width of leaf blade (WdLB) | -0.08 | 0.19 |
Length of scape (LgSc) | 0.08 | 0.33* |
Width of floral bract (WdFB) | 0.14 | 0.23* |
Length of floral bract (LgFB) | 0.29* | 0.08 |
Length of the sepals (LgSp) | 0.22* | 0.24* |
Length of fruit (LgFr) | -0.03 | 0.34* |
Width of fruit (WdFr) | 0.12 | 0.19 |
Length of seed (LgSd) | -0.03 | 0.29* |
Length of embryo (LgEm) | -0.01 | 0.25* |
Number of branches (NBr) | -0.03 | 0.09 |
Number of leaves per linear cm of shoot (NLS) | -0.22* | -0.08 |
Number of inflorescences per branch (NIB) | -0.04 | 0.09 |
Number of nerves in the floral bract (NNB) | 0.15 | 0.17 |
Number of nerves joined together at the apex of bracts (NNA) | 0.20 | 0.11 |
Fusion degree of the adaxial sepals (FDAd) | 0.27* | -0.14 |
Fusion degree of the abaxial sepals (FDAb) | -0.11 | 0.14 |
Type of stem (TySt) | -0.04 | 0.08 |
Leaf blade apex (LBAp) | -0.13 | -0.02 |
Arrangement of the leaf (ArLf) | 0.26* | -0.05 |
Type of leaf blade (TyLB) | 0.22* | -4.9E-03 |
Leaf sheath exposure (LSEx) | -0.27* | 0.10 |
Type of peltate hairs (TyPH) | 0.01 | 0.09 |
Winged hairs position in the leaf (WHPL) | -0.16 | 0.20 |
Pilosity of the leaf (PiLf) | -0.16 | 0.05 |
Scape position (ScP) | 0.06 | -0.13 |
Floral bract shape (FBSh) | 0.26* | 0.04 |
Floral bract apex (FBA) | 0.05 | -0.05 |
Floral bract indument (FBPb) | 0.29* | -0.14 |
Sepal dimension (SpSz) | 0.25* | -0.03 |
Sepal shape (SpSh) | 0.27* | -0.16 |
Endocarp shape (EnSh) | 0.05 | -0.06 |
Exocarp shape (ExSh) | -0.09 | 0.07 |
Quantitative analyses of reproductive and vegetative traits in the complex Tillandsia capillaris in Argentina. Box plots featuring medians (solid black square), means, and first and third quartiles (large box). Kruskal-Wallis (H) tests performed of selected characters are also included. Different letters above box-plots indicate statistical differences among taxa using a posteriori Dunn tests (p=0, 05) (
PCA for 5 different taxa of the Tillandsia capillaris complex. Plot of all specimens (100 OTUs) and leaning of the most influential 19 characters represented on the first two principal components resulting from principal component analysis (see Table 2 for abbreviations). References: OTUs: f. capillaris (n=21) =red; f. hieronymi (n=24) =blue; f. incana (n=20) =pink; f. virescens (n=12) =green; f. cordobensis (n=23) =orange.
PCoA showed that the two principal axes provide a clear ordination of the OTUs into three separate groups (Fig. 3). The two principal axes together account for 54.6% of the variability using the 19 characters previously selected in the PCA with coefficient >0.20 (Fig. 3). There is a clear distinction with a larger left-group formed by the Tillandsia capillaris f. capillaris, Tillandsia capillaris f. hieronymi and Tillandsia capillaris f. incana OTUs; a second central, upper-group formed by the Tillandsia capillaris f. virescens OTUs; and a third lower, right-group corresponding to the OTUs for Tillandsia capillaris f. cordobensis.
Many of the 19 most influential characters are useful to separate Tillandsia capillaris f. incana-hieronymi (=Tillandsia capillaris sensu Till) (Fig. 4a, b), Tillandsia capillaris f. cordobensis (=Tillandsia virescens s. str. sensu Till) (Fig. 4c, d) and Tillandsia capillaris f. virescens (=Tillandsia virescens s. l. sensu Till) (Fig. 4e, f). For example, characters such as: triangular and elongated floral bract; sepals long, acute and equaling the bract; elongated and curved leaf blades; and low number of leaves per linear cm of shoot are useful to delimit Tillandsia capillaris f. cordobensis.The second group formed by Tillandsia capillaris f. capillaris, Tillandsia capillaris f. incana and Tillandsia capillaris f. hieronymi can be circumscribed by: ovate-lanceolate sepals, exceeding in length the floral bract; round and wide floral bract; and straight and half-curved leaf blade. Finally, Tillandsia capillaris f. virescens (=Tillandsia virescens s. l.) has the smaller sizes of the fertile shoot, scape, leaf blade, fruit, seed, and embryo. This last form showed statistically similarities in some of the characters (length of the fertile shoot, scape and sepals; Figs 1a, d, f, respectively) with Tillandsia capillaris f. hieronymi. Nevertheless, the characters indument of the bract, shape of the sepals and fusion degree of the adaxial sepals allowed to separate the forms in two different groups (Fig. 2).
Principal coordinates analysis (PCoA) for 5 different taxa of the Tillandsia capillaris complex. Scatterplots of the first two axis based on 19 characters selected in the PCA and using the Gower distance (sqrt (1-S)). References: Characters used (see Table I); OTUs: f. capillaris (n=21) =red; f. hieronymi (n=24) =blue; f. incana (n=20) =pink; f. virescens (n=12) =green; f. cordobensis (n=23) =orange.
Infructescence structure in Tillandsia capillaris complex. a–b Tillandsia capillaris (=Tillandsia capillaris f. incana and Tillandsia capillaris f. hieronymi) a glabrous floral bracts much shorter than the sepals b the ovate-lanceolate sepals are partially fused c–d Tillandsia virescens s.str. (=Tillandsia capillaris f. cordobensis) c pubescent floral bracts equaling the sepals d the acute sepals are much more fused (60-90%) e–f Tillandsia virescens s. l. (=Tillandsia capillaris f. virescens) e pubescent floral bracts equaling the sepals, lacking scapes and violet capsules f the acute sepals are almost totally fused. Abbreviations: s=sepals; b=floral bract, bars=1 mm.
1 | Floral bracts glabrous. Sepals ovate-lanceolate, partially fused, exceeding in length the floral bracts | Tillandsia capillaris (=Tillandsia capillaris f. incana-hieronymi) |
– | Floral bracts pubescent or semi-pubescent. Sepals acute, almost totally fused, equaling or barely exceeding in length the floral bracts. | |
2 | Scapes developed (2–8 cm in length). Leaf blades elongated and curved, 2–6 cm long. Low number of leaves per linear cm of shoot (<4–5 leaves). Leaf sheaths widely visible. Sepals acute connated by 60–90% of their lengths, with 5–9 nerves. Floral bracts triangular and elongate | Tillandsia virescens s. str. (=Tillandsia capillaris f. cordobensis) |
– | Scape absent or scarcely developed (1-3.5 mm in length). Leaf blades straight and half-curved, shorter than 1 cm. Leaves per linear cm of shoot 5–11. Leaf sheaths barely visible. Sepals acute almost totally fused and with 1–3 nerves. Floral bracts round and wide | Tillandsia virescens s. l. (=Tillandsia capillaris f. virescens) |
The criteria used in previous classifications (
Among the characters analyzed, most were informative (approximately 63% of the quantitative and 44% of the qualitative characters). The quantitative characters are significant to separate groups, while the categorical characters were useful when the taxa had similar plant size (e.g. Tillandsia capillaris f. virescens and Tillandsia capillaris f. hieronymi). Within the non-informative qualitative characters, those referred to the peltate trichomes (TyPH, WHPL and PiLf) were cited in previous classifications (
Diagnostic characters used by
On the contrary, other diagnostic characters established by
Summarizing, our results partially support the classification of
All the forms analyzed are distributed in the central and northern Argentina, in the southern distributional range of the complex. The taxa Tillandsia capillaris (=f. incana- hieronymi) and Tillandsia virescens s. str. (=f. cordobensis), co-occur in almost the same sites and altitude levels. Tillandsia virescens s. str. was mentioned by
The main goal of this contribution was to analyze the available classifications of the Tillandsia capillaris complex using a relatively large sample of material with a multivariate perspective. This methodological approach allowed us to define three taxa in Argentina (Figs 3 and 4) with clear morphological limits, and to inquire into the conflicts between the available classifications. The next step is to compare these results using new material from other populations within the geographical range of the complex, specifically from Bolivia and Peru. We are not proposing new nomenclature combinations until the whole distribution area are investigated.
We thank Jorge Chiapella, Walter Till, and Sabina Donadío for useful taxonomic discussions on the complex. Also to Leonardo Versieux, Andrea Costa, Walter Till and Jorge Chiapella for helpful comments and suggestions of previous version of this manuscript. We are indebted to the curators of CORD, LIL, MA, W, and WU for access to plant material. We thank also to Marcelo Gritti that took some of the photographs. Financial support was provided by CONICET, SECyT (UNC), MINCyT and BMFW.