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Articles • Acta Bot. Bras. 29 (4) • Oct-Dec 2015 • https://doi.org/10.1590/0102-33062015abb0186   copy

Pollen morphology and its taxonomic significance in the genus Bomarea Mirb. (Alstroemeriaceae) - II. Subgenus Bomarea

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Abstract

Pollen morphology of 52 species (out of c. 79) of the Bomarea subgenus Bomarea was examined using light microscopy and scanning electron microscopy (SEM), or using SEM alone. The studied species of Bomarea were stenopalynous, characterized by large, oblate, monosulcate monads with reticulate exine sculpture in most species. Wide variation was observed in quantitative palynological features. The studied taxa were divided into four major groups based on exine ornamentation observed under SEM: microreticulate, reticulate, coarsely rugulate, and psilate-perforate. The reticulate exine sculpture may be a plesiomorphic character state for the genus Bomarea, and the coarsely rugulate and finely rugulate-perforate or psilate-perforate exine sculptures may have evolved independently more than once. In agglomerative hierarchical clustering (AHC) analyses of the genus Bomarea using quantitative pollen data, the studied species were distributed in either two (similarity-based) or four (dissimilarity-based) major clusters. Neither the recent molecular phylogenetic analyses nor the AHC analyses of Bomarea have recovered clades/clusters that represent traditionally recognized subgeneric taxa for the genus. Therefore, the most reliable infrageneric classification of Bomarea can be achieved by combining morphological, palynological, and molecular data from more extentive sampling of all the species.

agglomerative hierarchical clustering; Bomarea; exine sculpture; infrageneric classification; scanning electron microscopy

Introduction

Bomarea is the most diverse genus of Alstroemeriaceae, and it includes 100-120 species with a Neotropical distribution from Mexico in the north to Argentina/Chile in the south (Neuendorf 1977Neuendorf M. 1977. Pardiniae, a new section of Bomarea (Alstroemeriaceae). Botanical Notiser 130: 55-60.; Alzate 2005Alzate F. 2005. Three new species of Bomarea (Alstroemeriaceae) from the Andean region of Colombia. Novon 15: 253-258.). The genus is largely restricted to the Andean range and its continuation in Central America (Hofreiter & Tillich 2002Hofreiter A. 2008. A revision of Bomarea subgenus Bomarea s. str. section Multiflorae (Alstroemeriaceae) . Systematic Botany 33: 661-684.). Based on morphological features, the genus Bomarea is divided into four subgenera: Baccata (five spp.), Bomarea s. str. (c. 79 spp.), Sphaerine (12 spp.), and Wichuraea (18 spp.; Hofreiter & Tillich 2002). The subgenus Bomarea is characterized by a generally twining habit, with flowers pendulous and actinomorphic or horizontally oriented and zygomorphic, tepals deciduous, ovary inferior and dehiscent, and fruit leathery. Baker (1888)Baker JG. 1888. Handbook of Amaryllideae. London, George Bell & Sons. divided this subgenus into four main groups according to the structure of the inflorescence and the relation of the inner and outer tepals, and Killip (1935)Killip EP. 1935. New species of Bomarea from the Andes. Journal of the Washington Academy of Science 25: 370-377. later named these four groups Multiflorae, Caldasianae, Edules, and Vitellinae. Presently, four sections are recognized within the subgenus Bomarea: Multiflorae, Edules, Goniocaulon, and Pardinae (Harling & Neuendorf 2003Harling G, Neuendorf M. 2003. Alstroemeriaceae. In: Harling G, Andersson L. (eds). Flora of Ecuador. Vol. 71. Stockholm, Göteborg University. p. 3-108.; for details see Hofreiter 2008).

As part of a comprehensive survey of pollen morphology in the genus Bomarea, pollen studies of three subgenera, viz. Baccata, Sphaerine, and Wichuraea, have already been published (Sarwar et al. 2015Sarwar AKM Golam, Hoshino Y, Araki H. 2010. Pollen morphology and infrageneric classification of Alstroemeria L. (Alstroemeriaceae). Grana 49: 227-242. and references therein). Light microscopy (LM) was mainly employed in previous palynological studies of this genus, and scanning electron microscopy (SEM) was employed in a few cases (for details see Sarwar et al. 2015). We describe here, using both LM and SEM, the pollen morphological features of the subgenus Bomarea, and evaluate their usefulness for the infrageneric classification of this genus.

Materials and Methods

Pollen morphology of 52 species (out of c. 79) of the Bomarea subgenus Bomarea and of one species each of the subgenera Baccata and Wichuraea was examined by light microscopy (LM) and scanning electron microscopy (SEM), or by SEM alone (Tab. 1). Polliniferous materials used in this investigation were taken from dried specimens from the herbaria K, MO, MOL, NY, and USM. Herbarium abbreviations follow the Index Herbariorum (Thiers 2007Thiers B. 2007. Index Herbariorum: a global directory of public herbaria and associated staff. New York Botanical Garden's virtual herbarium. http://sweetgum.nybg.org/ih/. 27 Jan. 2015.
http://sweetgum.nybg.org/ih/... ).

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Table 1.
List of Bomarea taxa used in this study along with their voucher specimens. * New palynological data.

The pollen parameters studied and the LM and SEM preparation methods used follow Sarwar et al. (2010). Measurements were taken from at least 30 randomly selected grains from each specimen (Tab. 2). To visualize the relationships among the studied species of the subgenera Baccata, Bomarea, Sphaerine, and Wichuraea, agglomerative hierarchical clustering (AHC) analyses were conducted using the XLSTAT 2009.3 program, based on the quantitative characters polar length (P), equatorial diameter (E), P/E ratio, and exine thickness. The palynological data for the subgenera Baccata, Sphaerine, and Wichuraea were taken from Sarwar et al. (2015), and dendrograms were built using AHC. Slides of all specimens have been deposited in the Hokkaido University Museum, Sapporo, Japan. Pollen size and shape classes were defined using the criteria of Erdtman (1952)Erdtman G. 1952. Pollen morphology and plant taxonomy - Angiosperms. Leiden, E. J. Brill., and our descriptive terminology follows Punt et al. (2007)Punt W, Hoen PP, Blackmore S, Nilsson S, Le Thomas A. 2007. Glossary of pollen and spore terminology. Review of Palaeobotany and Palynology 143: 1-81. and Hesse et al. (2009)Hesse M, Halbritter H, Zetter R, Weber M, Buchner R, Frosch-Radivo A, Ulrich S. 2009. Pollen terminology: an illustrated handbook. New York, Springer.. The sectional classification of subgenus Bomarea follows Harling & Neuendorf (2003) and Hofreiter (2008).

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Table 2.
Variation in pollen characters of Bomarea subg. Bomarea showing mean value in micrometer and standard deviation. Minimum - maximum values in micrometer in parenthesis. Taxa are arranged alphabetically within the group. (A) Pollen grains with auriculae-like structures; n.d. Not discern.

Results

Based on LM and SEM observations, the Bomarea pollen grains studied were monad, large, ellipsoid (boat-shaped), heteropolar; monosulcate, sulcus on the convex part of the grain, distinct, long, straight, wide at the equator, narrow near the poles, sometimes extended to the proximal pole (Fig. 1A-D); auriculae-like structures at the end of the sulcus in B. acutifolia, B. amazonica, B. andreana (Croats 34872), B. bredemeyerana, B. cornigera, B. crocea, B. dispar, B. euryphylla, B. formosissima, B. hirsuta, B. lutea, B. macusanii, B. multiflora (Barclay 5295), B. suberecta, B. multipes, B. martiana, B. nematocaulon, B. pardina, and B. tarmensis (Fig. 1E-F; Tab. 2); opercula-like structures present on the sulcus in B. ovata (Fig. 1D). Symmetry is bilateral. Size ranges from 25.26-38.82 µm (polar length P) × 47.18-69.30 µm (equatorial diameter E), P/E 0.43-0.62, peroblate to oblate in shape, exine thickness 1.11-2.76 µm (Tab. 2).

Figure 1.
Light and scanning electron micrographs of Bomarea pollen. Pollen grains (A-F); exine sculpture (G-O). A. B. rosea (Ledezma et al. 710); B. B. crocea (Galiano et al. 6987); C. B. cochabambensis (Cutler 7678); D. B. ovata (Ferreyra 5300); E. B. multiflora (Barclay 5295); F. B. andreana (Croats 34872); G. B. amazonica (Barbour 2859); H. B. andreana (Davidson 7239); I. B. crassifolia (Fosberg 27845); J. B. hartwegii (Campos et al. 5735); K. B. multiflora (Feinsinger et al. 667); L. B. suberecta (Devidse et al. 28957); M. B. cornigera (Stein & Todzia 2230); N. B. edulis (Sarwar & Hoshino s. n.); O. B. multipes (Besse et al. 751). Scale bars: A-F, 10 µm; G-O, 1 µm. Specimen numbers are detailed in Tab. 1.

The pollen grains of Bomarea species were characterized by a semitectate exine sculpture. Four different exine sculpture types were observed:

Type I - Microreticulate (Figs. 1G-O, 2A-F; Tab. 2), with perforate muri, heterobrochate; lumina less than or equal to 1 µm in length or diameter; observed in B. amazonica, B. andreana (Davidson 7239), B. aurantiaca (Hawkes et al. 4438), B. boliviensis, B. cornigera, B. crassifolia, B. dispar, B. edulis, B. endotrachys, B. hartwegii, B. hirtella, B. martiana, B. multiflora (Feinsinger et al. 667), B. multipes, B. rosea, B. setacea (Jorgensen et al. 1373), B. suberecta, and B. peruviana.

Type II - Reticulate (Figs. 2G-O, 3A-O, 4A-F; Tab. 2), with perforate muri, heterobrochate; lumina larger than 1 µm in length or diameter; observed in B. acutifolia, B. anceps, B. andreana (Croats 34872), B. angulata, B. bredemeyerana, B. campylophylla, B. carderi, B. chiriquina, B. cochabambensis, B. cordifolia, B. cornuta, B. costaricensis, B. crocea, B. euryphylla, B. formosissima, B. goniocaulon, B. hirsuta, B. lopezii, B. lutea, B. macusanii, B. multiflora (Barclay 9394; Lepiz 217; Panafiel et al. 90; Barclay 5295), B. nematocaulon, B. ovata, B. patacocensis, B. patinii, B. perglabra, B. purpurea, and B. trichophylla.

Figure 2.
Scanning electron micrographs of Bomarea pollen. Exine sculpture (A-O). A. B. boliviensis (Wood 7818); B. B. dispar (Smith 6582); C. B. hirtella (Chagala 68); D. B. martiana (West 6114); E. B. rosea (Ledezma et al. 710); F. B. peruviana (Stein & Todzia 2033B); G. B. acutifolia (Davidse 24682); H. B. andreana (Croats 34872); I. B. bredemeyerana (Liesner et al. 7935); J. B. chiriquina (Mori & Kullunki 5651); K. B. costaricensis (Chavarria 663); L. B. crocea (Galiano et al. 6987); M. B. euryphylla (Palacios 6420); N. B. formosissima (Nunez et al. 8511); O. B. hirsuta (Chavarria 756). Scale bars: A-O, 1 µm. Specimen numbers are detailed in Tab. 1.

Figure 3.
Scanning electron micrographs of Bomarea pollen. Exine sculpture (A-O). A. B. lutea (Scolnik 1448); B. B. macusanii (Nunez et al. 8477); C. B. multiflora (Lepiz 217); D. B. multiflora (Barclay 9394); E. B. multiflora (Panafiel et al. 90); F. B. multiflora (Barclay 5295); G. B. patacocensis (Luteyn et al. 14078); H. B. patinii (Zarucchi et al. 5934); I. B. campylophylla (Miranda et al. 588); J. B. cordifolia (Foster & Smith 9076); K. B. cornuta (Stein & Todzia 2275); L. B. lopezii (Sagastegui 11402); M. B. ovata (Ferreyra 5300); N. B. angulata (Sagastegui 12759); O. B. goniocaulon (Hamilton & Holligan 522). Scale bars: A-O, 1 µm. Specimen numbers are detailed in Tab. 1.

Type III - Coarsely rugulate (Fig. 4G-I; Tab. 2); observed in B. aurantiaca (Cano 4679), B. pardina, and B. weigendii.

Type IV - Psilate-perforate (Fig. 4J-O; Tab. 2); observed in B. densiflora (Vigo 6229), B. obovata, B. setacea (Weigend et al. 97/405), B. superba, and B. tarmensis.

Figure 4.
Scanning electron micrographs of Bomarea pollen. Exine sculpture (A-O). A. B. perglabra (Løjtnant & Ulf Molau 13708); B. B. anceps (MOL2940370); C. B. cochabambensis (Cutler 7678); D. B. nematocaulon (Salinas 260); E. B. trichophylla (Berry 3273); F. B. carderi (Churchill 3904); G. B. aurantiaca (Cano 4679); H. B. pardina (Werff & Gudino 10794); I. B. weigendii (Tovar 5780); J. B. densiflora (Vigo 6229); K. B. setacea (Weigend et al. 97/405); L. B. superba (Farfan et al. 564); M. B. obovata (Vincelli 209); N-O. B. tarmensis (Stein & Todzia 2350). Scale bars: A-O, 1 µm. Specimen numbers are detailed in Tab. 1.

Granula were sometimes visible at the bottom of the lumina; these may correspond to "free standing columellae" (e.g. Fig. 1G; Hesse et al. 2009). The exine sculpture along with sulci was similar to that appearing at the equatorial position, but had relatively smaller lumina.

In agglomerative hierarchical clustering (AHC) analyses of the genus Bomarea using quantitative pollen data, the species studied were distributed in either two (similarity-based) or four (dissimilarity-based) major clusters (Fig. 5). Among these clusters, three include at least one species from each subgenus; cluster 1 (blue) comprises most of the taxa studied (41), cluster 2 (pink) comprises 12 taxa, cluster 3 (brown) comprises 16 taxa, and cluster 4 (black) comprises the single species B. ampayesana from the subgenus Wichuraea.

Figure 5.
Dendrogram obtained from quantitative data by agglomerative hierarchical clustering analysis. Names of species are abbreviated to the first four to six letters of the specific epithets.

Discussion

The Bomarea species studied were stenopalynous and characterized by monad, monosulcate, large pollen grains (Figs. 1-4; Tab. 2; Sarwar et al. 2015). The pollen morphology of 36 of these species, indicated by asterisks in Tab. 1, was studied for the first time using either LM or SEM. Our results are in agreement with previous reports (Erdtman 1952; Heusser 1971Heusser CJ. 1971. Pollen and spores of Chile. Tucson, University of Arizona Press.; Neuendorf 1977; Schulze 1978Schulze W. 1978. Beitragezur Taxonomie der Liliifioren III. Alstroemeriaceae. Wissenschaftliche Zeitschrift der Friedrich-Schiller-Universitat Jena/Thüringen, Mathematisch-naturwissenschaftliche Reihe 27: 79-85.; Kosenko 1994Kosenko VN. 1994. Pollen morphology of the family Alstroemeriaceae. Botanischesky Zhurnal 79: 1-8.; Sanso & Xifreda 2001Sanso AM, Xifreda CC. 2001. Generic delimitation between Alstroemeria and Bomarea (Alstroemeriaceae). Annals of Botany 88: 1057-1069.; Alzate 2007; Sarwar et al. 2015). The monophyly of the genus Bomarea is supported by molecular data (Aagesen & Sanso 2003Aagesen L, Sanso M. 2003. The phylogeny of the Alstroemeriaceae based on morphology, rps 16 intron, and rbcL sequence data. Systematic Botany 28: 47-69.; Alzate et al. 2008) and by the palynological data as well (Tab. 2; Sarwar et al. 2015). However, there were significant differences in the values of the quantitative palynological characters, which may to some extent be related to differences in the mounting media (Meltsov et al. 2008Meltsov V, Poska A, Saar M. 2008. Pollen size in Carex: the effect of different chemical treatments and mounting media. Grana 47: 220-233.) and the methods of preparation of the pollen grains (Schols et al. 2004Schols P, Es K, d'Hondt C, Merckx V, Smets E, Huysmans S. 2004. A new enzyme-based method for the treatment of fragile pollen grains collected from herbarium material. Taxon 53: 777-782.), as well as the species' geographical distribution, floral size, etc. (AKM Golam Sarwar pers. obs.). For example, there were significant differences between two B. andreana specimens, one of which had smaller pollen grains with a thinner exine (Davidson 7239, collected from the warmer region of Costa Rica), while the other had larger pollen grains with a thicker exine (Croats 34872, collected from the cooler region of Panama) (Tabs. 1, 2).

A wide and generally continuous pattern of variation in P, E, P/E ratio, and exine thickness was observed at both the infra- and inter-species level (Tab. 2). Among the sections of Bomarea subgenus Bomarea, section Goniocaulon produces pollen grains with relatively consistent P/E ratios (0.53-0.58) (Tab. 2). Pollen grain size within a genus is influenced by internal (chromosome number and floral character) and external (temperature, mineral nutrition, and water conditions) factors (Stanley & Linskens 1974Stanley RG, Linskens HF. 1974. Pollen: biology, biochemistry and management. Berlin, Springer-Verlag.). However, no correlation between ploidy level and palynological features was observed in Bomarea. The only tetraploid species of Bomarea, B. hirtella, produced pollen grains similar in size to or slightly smaller than the diploid species (Tab. 2; Cave 1967Cave MS. 1967. In: Documented chromosome numbers of plants. Madroño 19: 134-136.).

Auricula-like structures in pollen grains have been previously reported from only four Bomarea species, namely, B. brachysepala, B. bracteolata, B. glaucescens, and B. huanuco (Sarwar et al. 2015). In the present study, pollen with auricula-like structures was observed in 19 taxa (Fig. 1E; Tab. 2), including in B. ceratophora (Neuendorf 1977) in the subgenus Bomarea. These auricula-like structures may have some taxonomic importance for the genus Bomarea since they are relatively common in the subgenus Bomarea, but are completely absent in members of the southern group of the subgenus Wichuraea (Tab. 2; Sarwar et al. 2015). Auriculate pollen grains are not common among extant plant taxa, and diverse Cretaceous pollen-bearing auriculate appendages have been variously described as gymnospermous and monocotyledonous (Elsik 1974Elsik WC. 1974. Fossil auriculate pollen. Pollen Spores 16: 507-533.). As the term "auriculae" is only applicable to the spores' structure (Punt et al. 2007), the term "apex" has sometimes been used for these auricula-like pollen structures (see Martín et al. 2012 for detailed terminological discussion).

A recent molecular phylogenetic analysis of Bomarea (Alzate et al. 2008) identified three major clades, but none of them correspond to traditionally recognized subgeneric taxa (Hofreiter & Tillich 2002). Only seven of the species we studied were included in that molecular analysis, and these seven are positioned in two different clades (Fig. 2 in Alzate et al. 2008). Exine sculpture was found to be the most important palynological character possessing phylogenetic importance. In the molecular phylogenetic analysis, four members of section Multiflorae (B. vestita syn. B. multiflora; Hofreiter 2008) were included in clade C; this was also supported and confirmed by palynological characters, especially exine sculpture Type II (Figs. 2I, O, 3C-F; Tab. 2). The other species of section Multiflorae (B. setacea) are sister to clade B and are characterized by exine sculpture Type IV (Fig. 4K; Tab. 2), although wide variation was observed in the exine sculpture of two specimens of B. setacea (Type I vs. Type IV; Tab. 2), which may be due to polymorphism. Bomareasetacea is polymorphous taxon, especially in its general stature and in the shape and size of the leaves and inflorescence (Harling & Neuendorf 2003). Of the two other species of the subgenus Bomarea, B. edulis was included in clade A, and B. salsilla was sister to B. straminea (Fig. 2 in Alzate et al. 2008).

Pollen grains of Bomarea species are characterized by their (micro-)reticulate exine sculptures (Figs. 1G-O, 2, 3, 4A-F; Sarwar et al. 2015), although coarsely rugulate and finely rugulate-perforate or psilate-perforate exine sculptures are also observed in a few Bomarea species (Fig. 4G-O; Hofreiter 2008; Sarwar et al. 2015). This may give additional support to the supposition that (micro-)reticulate exine sculptures might be a plesiomorphic character state for Bomarea and the coarsely rugulate and finely rugulate-perforate or psilate-perforate exine sculptures might have evolved independently more than once (Alzate et al. 2008; Sarwar et al. 2015). These results may also confirm the major evolutionary trend in exine sculpture in the family Alstroemeriaceae from reticulate through rugulate-psilate to striate-reticulate, or vice-versa (Aagesen & Sanso 2003; Sarwar et al. 2010; 2015).

Among the quantitative pollen characters analyzed, equatorial diameter had the greatest influence on the position of taxa in the AHC cladogram (Fig. 5; Tab. 2; Sarwar et al. 2015). The members of cluster 1 commonly produced pollen grains 52.67-62.93 µm in size; cluster 2 produced relatively larger pollen grains (63.93-69.30 µm); cluster 3 produced the smallest pollen grains (44.46-55.30 µm). The large pollen grains of B. ampayesana (subgenus Wichuraea) might be one of the reasons for its very distinct position in cluster 4 (black) of the AHC (Fig. 5; Tab. 2; Sarwar et al. 2015). The greatest variation in pollen morphological features was observed in the subgenus Wichuraea (Fig. 5; Hofreiter & Tillich 2002), which also exhibited the greatest variation in other morphological features.

There were significant differences in the species composition of the different subclades/clusters recovered from both the molecular phylogenetic analysis (based on a few species; Alzate et al. 2008) and the AHC (based on quantitative pollen features; Fig. 5). Moreover, analyses based on different genomes (nuclear vs. plastid) not only lead to disagreements in the evolutionary relationships of taxa, but also greatly affected other phylogeny-based inferences and interpretations relating to taxonomy, morphological evolution, historical biogeography, and phylogenetic diversity (Zhang et al. 2015Zhang Q, Feild TS, Antonelli A. 2015. Assessing the impact of phylogenetic incongruence on taxonomy, floral evolution, biogeographical history, and phylogenetic diversity. American Journal of Botany 102: 566-580.). Therefore, the most reliable infrageneric classification of Bomarea will be achieved through combined analyses of morphological, palynological, and molecular data from more extentive sampling- of all the species in the genus.

Acknowledgements

We thank the directors and curators of the consulted herbaria for allowing us to examine or borrow specimens of polliniferous material. The first author is especially grateful to the Japan Society for the Promotion of Science (JSPS) for a Postdoctoral Fellowship for Foreign Researchers during the period of this study.

References

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    » http://sweetgum.nybg.org/ih/
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Publication Dates

  • Publication in this collection
    Oct-Dec 2015

History

  • Received
    15 July 2015
  • Accepted
    24 Sept 2015
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