ASPECTS OF '!HE EVOIDrIONARY BIOI.OOY OF THE PRCYI'EACEAE, WI'IH EMFHASIS ON THE GENUS IEUCADENDRON AND ITS FHYI.OGENY BY JEREMY JOHN MIOOIEY Submitted in part fulfilment of the requirements for the degree IX>CroR OF FHII.OSOPHY in the Department of Botany Faculty of Science University of cape Town March 1987 University of Cape Town The copyright of this thesis vests in the author. No quotation from it or information derived from it is to be published without full acknowledgement of the source. The thesis is to be used for private study or non- commercial research purposes only. Published by the University of Cape Town (UCT) in terms of the non-exclusive license granted to UCT by the author. University of Cape Town We shall not cease from our exploration And the end of all our exploring Will be to arrive where we started And know the place for the first time from: Four Quartets by T. s. Eliot TABIE OF OONl'ENTS Page Preamble 1 Chapter 1. 'Ihe derivation, utility and implications of a divergence index for the fynbos genus I.eucadendron 16 Chapter 2. 'Ihe distribution of the Proteaceae and their associated traits along a fynbos summer moisture stress gradient 45 Chapt;er 3. A biogeographical analysis of the genus I.eucadendron 68 Chapter 4. Factors which detennine, and ecological correlates of, maximum plant height of fynbos Proteaceae species 96 I., . Chapter 5 o '!he evolution of serotiny in the fynbos, with particular reference to the genus I.eucadendron (Proteaceae) 113 Chapter 6. '!he evolution of dioecy, with particular reference to I.eucadendron (Proteaceae) 143 Chapter 7. Factors which detennine why there are more species of seeders than sprouters in the fynbos Proteaceae 170 Chapter 8. What is the selective advantage of mynnecocho:ry in the Proteaceae? 203 Chapter 9. Ex:trafloral nectaries and leaf herbivo:ry in the Proteaceae 220 Chapter 10. Reproductive biology of the Proteaceae and inter-continental convergence 234 Conclusions Chapter 11. Should adaptationists consult the phylogenies of their study groups? 251 Chapter 12. Is climate as irrg;:>ortant as soil nutrients as an ecological detenninant of the fynbos flora and its characteristics? 269 1 PRF.AMBIE In this preamble I wish to set the scene for this thesis by briefly; i) explaining the reasons for my choice of subject matter and materials, ii) introducing the Fynbos Bi011l8 as hOll\8 to the studied taxon, iii) explaining my methods and justifying my approach, and iv) . giving a brief resume of each chapter and the main theses I could defend. SUbject matter '·· ·The questions which prorrpted this work are; i) what are the ecological and biogeographical distribution patterns of species of the Proteaceae, and their associated reproductive traits? ii) what is the adaptive significance of SOl1\8 of these reproductive traits? iii) can a phylogenetic perspective add to our understanding of the ecological and biogeographical reasons for various distribution patterns? iv) is climate or soil nutrient status, the dominant ecological and evolutionary detenninant of the fynbos? The fynbos flora Floristically the fynbos is characterised by shrubs of the Proteaceae, Rutaceae, Ericaceae and Asteraceae and an understorey of Restionaceae and cyperaceae, and only few grasses (Bond and Goldblatt 1984). The fynbos flora has an enonnous concentration of species (about 8500) in a very small area (67000km2 ; Goldblatt 1978). Structurally the fynbos is a heathland-shrubland characterised by sclero- 2 phyllous to microphyllous shrubs and aphyllous graminoids (Taylor 1978). The exact floristic and structural definitions are still being refined (campbell 1985). Reproductively, the fynbos is dominated by serotinous ("canopy stored seeds") (Kruger 1981) and myrrnecochorous ("ant-dispersed") (Bond and Slingsby 1983) obligate reseeding perenials (Kru.ger 1981). Geophytes are rn.nnerous and abundant, annuals are few and rare (Goldblatt 1978). '!he fynbos envirornnent The fynbos is restricted to a small, mainly mountainous, area of the southern and southwestern Cape. 'lhese folded mountains occur in two parallel ranges with an average height between 1 000 and 1 500m, and are mainly composed of sandstone and quartsitic rocks of the Table Mountain and Witteberg Series (Goldblatt 1978). '!he soils on the mountains are usually , coarse, acidic sands low in plant nutrients, particularly phosphate (Bond 1981). '!he climate of the fynbos is as varied as the to:EXJgraphy. Rainfall quantity varies from 300 to 2 500mm per anntnn {Taylor 1978). Rainfall seasonality ranges from winter in the west to all year in the east (Fuggle 1981) • Snow is conunon on the high peaks in winter. Why study reproductive ecology? 1) Most other gradient or geographic studies in the fynbos have centred on structural characters (Bond 1981; Cowling 1982; cantpbell 1985) • Reproductive biology is therefore a frontier of ecological knowledge. I have also investigated some vegetative characters (e.g. leaf size), to see whether 3 variation in these characters track various gradients better than do reproductive characters. Reproductive ecology is not only a new direction in fynbos research; the first general reviews on reproductive ecology have only appeared recently (e.g. Willson 1983). 2) Iynbos and other vegetation types are generally managed in tenns of the reproductive biology of the constituent elements. For managers to be able to conseJ::Ve conununities adequately, they need an understanding of repro­ ductive ecology. 'Ihe mountainous areas of the fynbos landscapes provides I•• I important water catc.hment areas. Management of the fynbos in these catchment areas is aimed at maintaining high quality runoff and species diversity, by applying burning at various periodicities and seasonalities. An understanding of the ecological effect of fires of different perio­ dicities, seasonalities and intensities, can only be atterrpted with an understanding of reproductive ecology. As a response to the need for an understanding of reproductive ecology, most of the chapters of this thesis concern reproductive attributes such as seed size, pollination type, seed storage type, regeneration mode and breeding systems. Why study the Proteaceae? Most of our present understanding of the response of the fynbos flora to fire is based on the Proteaceae (Jordaan 1981; Bond, Vlok and Viviers 1984; Midgley and Vlok 1986). '!he following are some of the many reasons for the concentration of effort on the Proteaceae; i) their taxonomy and field identification is easy, 4 ii) there are many (320) species and they are widely distributed throughout the biome, iii) they exhibit almost the full range of reproductive traits, iv) they are long lived and the most conspicuous element in mature fynbos, v) they are sensitive to fires of different seasonalities or frequencies, vi) .identifiable remains survive fires. and are present in burned vegetation for a few years after fire, and vii) they can be readily aged. For these reasons, I decided to investigate a genus within this family. I I reasoned that by studying a single taxon I would be able to discern patterns at evolutionary, biogeographic and ecological levels. Also I was frustrated with having to learn many new names, when wanting to "botanise" in any new fynbos area. 'lhe taxon I was looking for was preferably to be composed of many species, to be widespread enough to be represented in all the geographic regions of the fynbos and, to have representatives of the main reproductive strategies present in the fynbos. '!he genus Leucadendron, possibly uniquely, satisfies the criteria I had in mind. Without initially realising the enonnous ecological diversity of the genus, I was inunediately attracted to the genus after reading Williams's (1972) excellent revision. 'lhe following are some of the attributes of the genus; i) it is the genus of the Proteaceae with the most extant fynbos species (79), ii) the genus is well distributed throughout the fynbos biorne, iii) it is the only genus with species which are rnynnecochorous, serotinous, 5 or have passive soil stored seeds. '!his diversity of seed storage mechanisms may well be unique in the world, because a genus 'Which has even two of these strategies is remarkable. iv) some species can resprout after fire, v) seed size varies by orders of magnitude within the genus, vi) the genus is dioecious and has wind pollinated elements (both rare conditions in the family), and vii) the genus has extrafloral nectaries. surprisingly no ecologist had previously focused on this amazing genus. '·· ·· F\lrt:hennore, the taxonomy of the genus is well Jmown thanks to the meticulous work of Williams (1972). MEIHODS 'Ihe correlative or comparative methcd , Initially, I was concerned with questions like "'Why be serotinous" and "what does the ecological distribution pattern of most serotinous species indicate about the adaptive significance of serotiny"? 'Ibis type of approach, in 'Which mnnbers of species 'Which exhibit various traits (such as serotiny) are correlated with ecological factors (e.g. degree of moisture stress), has been widely used in biology. Although most of the characters I investigated have not been previously considered in the fynbos, some have been investigated with the correlative method in other areas; such as Baker's (1972) and Rock.wood's (1985) study of seed weight and Fox's (1985) study of dioecy, in 'Whole floras. Besides the correlative approach I perfonned some field and laboratory 6 experiments (e.g. gennination rates, exclusion trials) where necessary. I also collected data from field obsei:vations (e.g. sex ratios). I hoped the correlative method would give an evolutionary perspective of reproductive traits, to compliment the experimental approach. However, it became more and more apparent that the results of the correlative method at the interspecific level are difficult to interpret. I was troubled by factors such as; because most serotinous species have winged seeds, was dispersal a major factor involved in the evolution of serotiny? It became I '· necessary, therefore, to consider whether winged seeds evolved before or after the trait of serotiny.