Title Pollen Morphology and Its Systematic Significance in the Ericaceae Author(s) Sawara, A.K.M. Golam Citation 北海道大学. 博士(農学) 甲第8187号 Issue Date 2007-03-23 DOI 10.14943/doctoral.k8187 Doc URL http://hdl.handle.net/2115/46925 Type theses (doctoral) File Information sarwar.pdf Instructions for use Hokkaido University Collection of Scholarly and Academic Papers : HUSCAP Pollen Morphology and Its Systematic Significance in the Ericaceae (ツツジ科植物の花粉形態とその体系学的意義) A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy By Sarwar, A.K.M. Golam Division of Bioresources and Product Science Graduate School of Agriculture Hokkaido University Sapporo, Japan March, 2007 Contents Abstract iv Chapter 1: GENERAL INTRODUCTION 1 Chapter 2: MATERIALS AND METHODS 10 Chapter 3: POLLEN MORPHOLOGY AND ITS SYSTEMATIC SIGNIFICANCE 20 GENERAL POLLEN MORPHOLOGY OF THE ERICACEAE 20 3-1 SUBFAMILY ENKIANTHOIDEAE 24 Introduction 24 Results 25 Discussion 30 3-2 SUBFAMILY ARBUTOIDEAE 44 Introduction 44 Results 45 Discussion 51 3-3 SUBFAMILY ERICOIDEAE 60 Introduction 60 Results 61 Discussion 81 3-4 SUBFAMILY CASSIOPOIDEAE 106 Introduction 106 Results 107 Discussion 110 ii 3-5 SUBFAMILY HARRIMANELLOIDEAE 112 Introduction 112 Results 113 Discussion 113 3-6 SUBFAMILY VACCINIOIDEAE 118 Introduction 118 Results 119 Discussion 160 Chapter 4: GENERAL DISCUSSION 203 Acknowledgements 252 Summary 254 References 259 Appendix I: Different classification systems of Ericaceae 281 Appendix II: Specimens examined 287 iii Abstract A detailed description of the range of pollen morphological variation within the family Ericaceae sensu Kron et al. (2002a) has been presented. For this palynological investigation, 275 taxa of 270 species representing 57 genera and 6 subfamilies were studied with light (LM) and scanning electron microscopy (SEM), and 31 species with transmission electron microscopy (TEM). The systematic significance and evolutionary trends of palynological characters have been discussed in the light of the recent phylogenetic classification of the Ericaceae. Pollen grains are dispersed as monads, tetrads or polyads, commonly of medium (30 – 50 µm) size and 3-colpor(oid)ate. Viscin threads are present only in a few genera of the subfamily Ericoideae (Bejaria and other eight genera). With SEM, exine sculpture varies from finely verrucate to psilate, and twelve major exine sculptural types have been recognized. Two dichotomous keys to the pollen of Ericaceae were prepared with the characters observed under LM, and exine sculpture with SEM. With TEM, the exine structure of ericaceous pollen is basically the same, and composed of sexine; tectum and columellae and nexine; foot layer and endexine. Two unique exine structures, granular columellae and canalized tectum, were observed in the monad pollen of two Erica species, E. barbigera and E. recurvifolia, and the tectum with (a few) canals also observed in Rhododendron japonicum and Oxydendrum arboreum. The TEM observations were also found useful to confirm some critical palynological observations with LM and/or SEM: heterodynamosporus tetrads, different types of exine sculpture, tetrads without septa, presence of pollenkitt and pollenkitt ropes, cause of pollen shrinkage, and identification and realignment of taxa. The family Ericaceae is eurypalynous enough to clarify the differentiation of species and genera, but has limited potential for clarification of the demarcation and relationships of higher taxa (e.g., tribes). Generally, the recent classifications and relationships among the iv genera of Ericaceae were supported by results of the present study. Qualitative palynological characters (e.g., exine sculpture) were found to be taxonomically more important than quantitative characters (e.g., tetrad diameter), and various palynological characters important for different taxonomic levels. Palynological features were also found to be significant in some infrageneric classifications (e.g., Arctostaphylos), and to identify the monophyly of taxa (e.g., Dimorphanthera). Moreover, some taxonomic problems were presented, and realignments of some taxa have been suggested from the palynological view point, e.g. tribal limits of the tribe Bejarieae. Individual generic status of the following three taxa has been proposed: Erica recurvifolia E.G.H. Oliv. as Eremia recurvata Klotzsch; Rhododendron tsusiophyllum Sugim. as Tsusiophyllum tanakae Maxim.; and Vaccinium japonicum Miq. as Hugeria japonica (Miq.) Nakai. At least one misplaced species was also identified; Enkianthus sikokianus (Palibin) Ohwi should be recognized as a separate species, but it has been incorporated into E. campanulatus (Miq.) Nicholson. The present study revealed a number of evolutionary trends in different palynological features viz., pollen dispersal units, compactness of tetrads, pollen size and shape, aperture number and exine sculpture, within the family Ericaceae as well as within a genus (e.g., Enkianthus), and suggestions were made concerning the selective value of some of these trends. There is no clear correlation between pollen features of the family Ericaceae and either pollinators or geographical distributions, but present in lower taxa (e.g., Rhododendron, Erica). In the course of the pollen survey the following interesting discoveries were made: the first unique palynological feature – pollen tetrads without septa for the Ericaceae (e.g., Ceratostema) as well as other angiosperm families; the parallel evolution of pseudomonad pollen tetrad development in the subfamily Styphelioideae and Vaccinioideae; pollenkitt ropes were found on the dried herbarium specimens (e.g., Notopora); and pollen tetrads with four aperturate grains were discovered in a number of taxa (e.g., Vaccinium). v Chapter 1 General Introduction The Heath family Ericaceae is the 8th largest family of angiosperms, it comprises eight subfamilies, approximately 125 genera and 4100 species (Kron and Luteyn 2005). It is widespread in temperate, cool, and subtropical regions and in tropical regions in the mountains (Fig. 1-1). The Ericaceae has many fruit and timber yielding genera, many are valuable as showy ornamentals and sources of essential oils. Members of this family are highly diverse in life forms, leaf morphology, inflorescence characteristics and palynological features. Pollen grains of this family are dispersed as monads (e.g., Enkianthoideae) vs. tetrads – commonly isodynamosporus (all four grains of the same size, Erdtman 1952) or heterodynamosporus (all four grains not of the same size, Erdtman 1952) (e.g., Styphelioideae); or as polyads of indefinite number of tetrads (e.g., Chimaphila). The variety of pollen types, which are unparalleled by any other angiosperm family, makes the Ericaceae unique (Venkata Rao 1961). Pollen tetrads of this family sometime possess very rare and unique characters viz., 4-aperturate grains, pollenkitt ropes in dried herbarium specimen (e.g., Notopora), and completely absence of septal (partition) wall between the two neighboring grains (e.g., Ceratostema), among the angiosperms. The last classifications of the Ericaceae on a world basis were those of Hooker (1876) and Drude (1889). These have been accepted by the most subsequent workers as a satisfactory basis for discussion, proposing only minor modifications. However, subdivisions within Ericaceae and recognition of segregate families, Monotropaceae and Pyrolaceae varied with different authors (Table 1-1, detail in Appendix 1). Affinities of the Ericaceae with other families have also been variously discussed (e.g., Drude 1889, Takhtajan 1997). 1 A. Enkianthoideae (1/16) B. Monotropoideae (15/50) C. Arbutoideae (4/81) D. Cassiopoideae (1/12) E. Ericoideae (19/1780) F. Harrimanelloideae (1/2) G. Styphelioideae (35/520) H. Vaccinioideae (45/1593) Fig. 1-1. World-wide distribution maps for the eight subfamilies of the Ericaceae. A. Enkianthoideae; B. Monotropoideae; C. Arbutoideae; D. Cassiopoideae; E. Ericoideae; F. Harrimanelloideae; G. Styphelioideae; H. Vaccinioideae. In parenthesis no. of genera/ no. of species. Adapted from Kron and Luteyn (2005). 2 Table 1-1: Comparison among the outline of the major classifications of Ericaceae Engler & Prantl (1889, 1891) Stevens (1971, only Ericaceae) Hutchinson (1973) Cronquist (1981) Kron et al. (2002a) Order Ericales Order Ericales Order Ericales Order Ericales Order Ericales Family Pyrolaceae Family Ericaceae Family Pyrolaceae Family Empetraceae Family Ericaceae s.l. Pyroloideae Rhododendroideae Family Ericaceae Family Epacridaceae Enkianthoideae Monotropoideae Ericoideae Family Prionotaceae Family Ericaceae Monotropoideae Family Ericaceae Vaccinioideae Family Epacridaceae Family Pyrolaceae Arbutoideae Rhododendroideae (including Arbutoideae) Family Monotropaceae Family Monotropaceae Ericoideae (incl. Empetraceae) Arbutoideae Pyroloideae Family Vacciniaceae Cassiopoideae Vaccinioideae Monotropoideae Order Celastrales Harrimanelloideae Ericoideae Wettstenioideae Family Empetraceae Styphelioideae (incl. Epacridaceae) Family Epacridaceae Vaccinioideae Order Sapindales Family Empetraceae 3 With the improvement of large data analysis techniques and advancement of molecular systematics, interest on the systematics of this family has significantly increased in the past two decades. Recently a revised phylogenetic classification of the Ericaceae has been proposed (Kron et al. 2002a, Fig. 1-2), which recognizes 8 subfamilies and 20 tribes, and Cyrilla (Cyrillaceae) as the sister to the Ericaceae.