Pollen diversity in the genus Carlina L. (subtribe Carlininae, Compositae) and its systematic significance

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Highlights

  • Pollen morphology of 24 taxa of Carlina was observed and studied by LM and SEM.

  • HCA and PCA analyses applied to detect the potential characters separating the taxa.

  • Dichotomous keys to pollen types of the studied taxa of Carlina were constructed.

  • Qualitative and quantitative pollen characters can easily separate the Carlina taxa.

  • ImageJ program is a useful tool in measuring the quantitative of pollen characters.

Abstract

Pollen morphology of 19 species, 4 subspecies, and 1 variety of Carlina was studied in detail by light and scanning electron microscopy. Qualitative and quantitative pollen morphological characters which vary between taxa are found in the length of the ectocolpi, presence/nature of the echinae, pollen size and shape, lumina area, P/E ratio, polar axis, equatorial diameter, pollen shape, ectocolpi length, sculpture of ectoaperture membranes, area of lumina, and exine ornamentation. Three main pollen types are discerned: the C. atlantica type characterized by P/E ≤ 1.00, the C. curetum type characterized by P/E = 1.03–1.11, and the C. acanthifolia type with ratio P/E = 1.24–1.50. HCA and PCA analyses were carried out to detect the potential palynological characters which could be used to identify taxa. The data suggest that several pollen morphological characters can be used to delimit the taxa of Carlina. Dichotomous artificial keys based on palynological data are also given.

Introduction

Carlina L is a well-defined genus belongs to the tribe Cardueae, subtribe Carlininae of Compositae. The Cardueae are known commonly as “thistles” and plants of Carlina are known as “carline thistles.” The genus is medium-sized, comprising a number of species and infrageneric taxa with estimates of 28 species, 12 subspecies, and 14 varieties according to Kovanda (2002) and Susanna and Garcia-Jacas (2007), and 34 accepted species, 12 subspecies, and 7 varieties, according to The Plant List (2013). The genus is distributed from the Canary Islands and the Mediterranean (across Europe and northern Africa) to temperate Asia (central Siberia and northwestern China) (Kovanda, 2002, Peng et al., 2012). Meusel and Kästner (1994) divided the genus Carlina into five subgenera, Carlina, Carlowizia, Heracantha, Lyrolepis, and Mitina, with an underlying hierarchy of sections and subsections.

In their monograph of the genus, Meusel and Kästner, 1990, Meusel and Kästner, 1994 provided a review of Carlina that covered their leaf morphology, inflorescence, flower and fruit, chorology, ecology, karyology, embryology, palynology, chemistry of secondary compounds, and taxonomy. A molecular phylogeny of the genus has been established (Susanna et al., 2006, Wahrmund et al., 2010).

Palynological studies have been helpful tools in taxonomical revisions of numerous genera of Compositae and the Cardueae in particular (Bolick, 1978, Bordbar and Mirtadzadini, 2015, De Leonardis et al., 1984, Garnatje and Martín, 2007, López, 1981, Osman, 2009, Ozler et al., 2009, Pehlivan, 1995, Petit et al., 2001, Punt and Hoen, 2009, Shabestari et al., 2013, Skvarla et al., 1977, Skvarla and Turner, 1966, Stix, 1960, Velari, 1982, Wagenitz, 1976, Wagenitz, 1955).

To date details of pollen morphology are limited to only a few species of Carlina as part of studies at the family and tribal level and in the description of certain species (Beug, 2004, Dimon, 1971, Dittrich, 1977, La-Serna Ramos et al., 1999, Meusel et al., 1984, Petit, 1997, Punt and Hoen, 2009, Stix, 1960, Terrab et al., 2001, Tormo et al., 1984, Valdés et al., 1987).

In this study, we detail pollen morphological characters of 24 taxa of Carlina (19 species, 4 subspecies, and 1 variety). From this data set we assess pollen morphological support for the current infrageneric classification of Carlina. Provision of an identification key to species using pollen is aimed at further applications in other taxonomic studies as well as expanding the palynological knowledge base of the Compositae.

Section snippets

Pollen materials

Pollen grains of the studied species of Carlina were extracted from fertile anthers of flowers in anthesis and/or from buds in pre-anthesis, derived from 26 herbarium specimens of 24 taxa deposited in MSB Herbarium at the Ludwig–Maximilians–Universität München, Germany (herbarium acronyms follow Thiers, 2017) (Table 1). Nomenclature of the studied species was updated according to APG III (2009) and the Kew Garden plantlist website (The Plant List, 2013).

Light microscopy (LM)

For light microscopy, pollen material was

General pollen morphology

Pollen grains of the studied taxa of Carlina are quite homogeneous in their characters. Main features of the analyzed pollen grains of 19 species, 4 subspecies, and 1 variety of Carlina are summarized in detail in Table 2, Table 3, Table 4, Table 5 and Plate I, Plate II, Plate III, Plate IV, Plate V.

Pollen grains are monads and 3-zonocolporate. Most of the studied taxa of Carlina have a sub-spheroidal shape. Among other taxa, prolate (C. acanthifolia, C. biebersteinii subsp. brevibracteata, C.

Discussion

Pollen of the taxa of Carlina studied are consistently 3-zonocolporate monads with elongate ectoapertures and echinate ornamentation. The taxa are diverse in shape (sub-spheroidal, sub-prolate, prolate, or prolate-spheroidal), polar view area (small, medium, or large), length of ectocolpus, tectum ornamentation pattern, and P/E ratio. These results are in agreement with the findings of Tormo et al. (1984) and Punt and Hoen (2009).

Although morphologically pollen grains of the studied taxa of

Conclusion

This study contributes to the understanding of pollen diversity in Carlina with substantial variation across a range of characters. The palynological characters of the studied taxa serve for the identification and classification of taxa at the specific level. The qualitative and quantitative pollen characters provide a helpful taxonomic key for the isolation of closely related species. Further work will be required to determine if the significant differences between single samples of the

Declaration of Competing Interest

The authors declare that there is no conflict of interest regarding the publication of this article.

Acknowledgments

We would like to express our deep gratitude to the director of MSB Herbarium for allowing the study of their specimens. Sincere thanks to Dr. Murray Fagg, Australian National Herbarium & Australian National Botanic Gardens, Canberra, Australia, Dr. W.R. (Bill) Barker and Dr. Robyn Barker, the State Herbarium of South Australia for their diligent proofreading and comments which improved this manuscript. Sincere thanks and deepest appreciation to Dr. Jennifer A. Tate, Senior Lecturer in Plant

References (50)

  • W. De Leonardis et al.

    Premiere contribution à l’étude taxonomique du genre «Centaurea» de la Sicile sur la base des données polliniques, traitées par l’analyse informatique

    Webbia

    (1984)
  • M.-T. Dimon

    Problèmes généraux soultevés par l’étude pollinique de Composées Méditerranéennes

    Nat. Monspel. Ser. Bot.

    (1971)
  • M. Dittrich

    Cynareae -systematic review

  • G. Erdtman

    The acetolysis method—a revised description

    Sven. Bot. Tidskr.

    (1960)
  • G. Erdtman

    Handbook of palynolgy: Morphology, taxonomy, ecology. An introduction to the study of pollen grains and spores

    (1969)
  • G. Ferrauto et al.

    Pollen diversity in the genus Ptilostemon (Asteraceae, Cardueae) from Italy and its taxonomic and palynoecological implications

    Plant Biosyst.

    (2017)
  • T. Garnatje et al.

    Pollen studies in the genus Echinops L. and Xeranthemum group (Asteraceae)

    Bot. J. Linn. Soc.

    (2007)
  • H. Halbritter et al.

    Illustrated Pollen Terminology

    (2018)
  • M. Kovanda

    Observations on Carlina biebersteinii

    Thaiszia - J. Bot. Košice

    (2002)
  • I.E. La-Serna Ramos et al.

    Pollen characterization of multifloral honeys from La Palma (Canary Islands)

    Grana

    (1999)
  • R.C. Lopes et al.

    Pollen morphology and wall structure of Neotropical species of Herreria and Clara (Asparagaceae-Agavoideae) and its taxonomic implications

    Plant Syst. Evol.

    (2013)
  • López, G.B., 1981. Estudios taxonómicos en el género Centaurea L. sección Willkommia G. Blanca. Palinol. Bot. Macaron....
  • H. Meusel et al.

    Lebensgeschichte der Gold-nod Silberdisteln Monographie der mediterranmitteleuropäischen Compositen-Gattung Carlina

  • H. Meusel et al.

    Lebensgeschichte der Gold-und Silberdisteln Monographie der mediterran-mitteleuropäischen Compositen-Gattung Carlina

  • A.K.E. Osman

    Palynological studies on the Egyptian species of Compositae (subfamily Cichorioideae) and its taxonomic significance

    (2003)
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