Refuge Begonias : taxonomy, phylogeny and historical biogeography of Begonia sect. Loasibegonia and sect. Scutobegonia in relation to glacial rain forest refuges in Africa

Abstract

Begonia is a genus of + 1000 species and is represented in all tropical areas. In Wageningen, under the guidance of dr J.J.F.E. de Wilde, the continental African begonias are being studied. Continental Africa has some 120 species, divided over 10 sections, and compared with the amount of species on other continents it is poor. A study on two of those sections with a total of 40 species is recorded in this work. The status of these species was in urgent need of revision, and it was questionable whether the two sections could be upheld.Some other important research questions are related to the theory on glacial rain forest refuges.The taxonomic level achieving the rank of section or genus is rather arbitrarily defined and it is being applied differently throughout the plant kingdom.In this study, species are approached according to the biological species concept. Subspecies are regarded as evolutionary entities separated in space, while varieties occur sympatrically.An extensive morphological study is the basis for distinguishing the separate species. The two sections are characterized a.o. by a creeping rhizome, a monochasial inflorescence with strongly reduced axes, indehiscent fruits, and male and female flowers with 2 perianth segments that are often bright yellow. Important diagnostic features for the separate species are found in the shape of the ovary and in the shape and the indumentum of the leaves. No clear delimitation between the two sections could be made on the basis of exclusively macromorphological characters (but see below).Former studies revealed a wide variety of leaf anatomical characters within Begonia. A leaf anatomical investigation of the species treated here was performed. Its primary objective was to acquire supplementary characters for the phylogenetic analysis, in order to obtain a more concrete and broader basis. The second objective was to investigate whether anatomical differences between the two sections could be identified.Leaf anatomy was studied by means of electron microscope research and the analysis of transverse sections. The results are considered to be satisfactory, as both goals mentioned above were reached. It was demonstrated that even within this group of closely related species a wide variety of anatomical characteristics exists, which in many cases support phylogenetic relationships already advanced upon the results of the macromorphological study.Important leaf anatomical characters are:- the presence or absence of a cuticula structure on the hairs,- the presence of short, sausage-shaped, often clustered glandular hairs or of longer, solitary, r-shaped ones,- the presence of sclerenchyma around the vasculary bundles,- the size of the epidermal cells in relation to that of the cells of the palisade parenchyma below them.Some leaf anatomical characters may be regarded as adaptations to the often deeply shaded habitat conditions in which the plants grow naturally.Anatomical characteristics of the ovary were investigated and also used for the phylogenetic analysis. Some important ones are the shape of the placentae, the shape of the septa and the arrangement of the ovules.The vascularisation within the ovary was analysed through series of cross sections. Former research suggested the activity of 2 separate meristems in shaping the ovary. This view was supported by research performed at Wageningen on the vascularisation within species of the section Tetraphila. The vascularisation of the species studied here does, however, not support this hypothesis and suggests a 'normal' development from carpels.The anatomical structure of papillae on the style also shows variation which is indicative for common descent.Micromorphological characters of the seeds were investigated earlier by colleagues in Amsterdam and they proved to be useful in delimiting sections within the genus Begonia. Some relevant characters were selected and added to the datamatrix used in the phylogenetic analysis.Species of the sections studied here have been artificially hybridized in the past, both mutually and with species from quite different sections. Some putative natural hybrids have also been observed. In only one case this possibly concerned hybridization with a species from a different section, viz. the closely related Filicibegonia.Most species of the sections Loasibegonia and Scutobegonia grow on medium to heavily shaded sites in humid tropical rain forest. They are terrestrial and occur on comparatively acid, often clayey soils with a low Mg-content.Many of the species are difficult to cultivate and demand a high relative humidity, a light, comparatively acid substrate and protection against direct sunlight.Generally, the species flower during distinct periods, usually twice a year. The flowers of several species show sleeping movements and are closed during parts of the day and night. It is still quite uncertain how pollination takes place, although insect pollination is the most likely possibility. Maturation of the fruit often takes several months. The seeds are released close to the mother plant from slowly disintegrating fruits and seed dispersal therefore does not seem to be very effective.Taxonomy strives after a stable and natural system of classification. A strict reflection of genealogical relationships in nomenclature is not compatible with its stability. The acceptance of a certain kind of paraphyletic clades as genera offers a solution.Most likely the two sections studied here form together a monophyletic group. The section Filicibegonia represents the most plausible outgroup.On account of a theoretical presupposition, a particular treatment of polytypic characters in a phylogenetic analysis is being proposed.A datamatrix for the 40 species and 132 characters was drawn up and analysed by means of cladistic methods. A first analysis yielded a very instable result with a comparatively large amount of 'weak' characters. That is why a weighting method was developed and applied. It diminishes the influence of 'weak' characters on the final cladogram structure. After application of this method 7 monophyletic subgroups could be identified. In addition, two of those were analysed separately in order to reveal their ingroup structure. The definite position of 5 species remained uncertain. The ultimately accepted phylogenetic tree is less parsimonous than the initial one.The most important conclusion that may be drawn from the genealogical relations is, that the sections Loasibegonia and Scutobegonia represent 2 monophyletic groups and therefore they should be upheld. Synapomorphic characters for the section Loasibegonia are the juicy petioles and the short, sausage- shaped glandular hairs. The presence of a thin epidermis, sclerenchyma around the tertiary nerves, a cuticula structure on the hairs, long r-shaped glandular hairs and an obtuse operculum of the seed is characteristic for species belonging to the section Scutobegonia.During the last glacial (± 70,000 - 12,000 year B.P.) in tropical Africa it was considerably cooler, + 4°C, and there was much less precipitation than at present. As a result the area of lowland rain forest presumably shrank considerably and ultimately disintegrated into a number of small refuges, situated as islands within an area occupied by more drought-resistant vegetation. Under these circumstances the area of montane rain forest probably expanded locally. Consequently, when speaking of rain forest refuges, one must make a clear distinction between lowland and montane rain forest.The Begonia species studied here are practically all confined to shaded, humid places in tropical lowland rain forest. During the last glacial, they will have survived almost exclusively in the refuges. Since, moreover, their seed dispersal seems not to be very effective, the location of the former refuges may be deduced from their present-day distribution.Begonia taxa happen to occur concentrated indeed within the main refuge localities postulated by other researchers, viz. in Liberia/Ivory Coast, in Cameroon/Gabon and in eastern Zaire. Within the Cameroon/Gabon area some 5 or 6 smaller areas with a high number of endemics can be denoted. These coincide remarkably well with the areas earlier indicated as possible refuges on the basis of other data. This strong conformity supports the view that these begonias may be regarded as dependable indicators of former refuges. As such they point to the possibility that also the Mayombe area and possibly the Doudou Mountains represent former lowland rain forest refuges.The existance of geographically isolated refuges formed a stimulant for speciation processes. Because of their short life cycle and the plasticity of their characters, the present species should be capable to evolve rapidly. Whether this has indeed happened under the influence of the development of refuges is an important question, that is studied next by means of a historical biogeographic analysis.Because it is plausible that the localities of former refuges will have retained a high degree of biodiversity into our days, knowledge about their location is of prime importance for nature conservation activities.By means of historical biogeographical research it is attempted to reconstruct the geological and climatological developments, using the phylogeny in combination with the distribution patterns of taxa. Nowadays, cladistic methods are often used, and among these Brooks Parsimony Analysis is considered theoretically the most suitable.In all, 25 areas of endemism have been demarcated. A first analysis lead to a poor result due to the comparatively large quantity of areas lacking their own endemic Begonia taxa. Eliminating these areas from the analysis yielded a better result, which was, however, still not optimal owing to the uncertain position within the areagram of the Doudou Mountains. Disregarding the latter area yielded an acceptable result. Eliminating areas seems to lead to good results in the present case, but the precise theoretical consequences of such actions need to be further investigated.A core area, composed of some 5 areas in Cameroon and Gabon, can be identified in all analyses that were performed. It coincides comfortably with the 'Lower Guinea' region often cited in floristical studies.Because the analyses show that sister species rarely occupy adjacent areas, remarkably few vicariance events seem to have occurred. If vicariance did occur during the last and previous glacials, this is perhaps concealed at present because of renewed dispersal after each occasion. The relationships between the areas seem to be more of a reflection of floristic similarity, rather than of a common history.There are indications for the presence of a demarcation line along the Sanaga River and another one across Equatorial Guinea.A revision of the sections Loasibegonia and Scutobegonia, including a key to the taxa, is presented. The taxa are accompanied by extensive descriptions, drawings, distribution maps, ecological notes and other relevant data. Recently, 14 new species have been published. In the present work the following additional new taxa are described and new combinations proposed:Begonia letouzeyi SosefBegonia prismatocarpa W.J. Hooker subsp. delobata SosefBegonia prismatocarpa W.J. Hooker subsp. petraea (A. Chev.) SosefBegonia quadrialata Warb. subsp. quadrialata var. pilosa SosefBegonia quadrialata Warb. subsp. nimbaensis SosefBegonia quadrialata Warb. subsp. dusenii (Warb.)Sosef Begonia scapigera Hook.f. subsp. australis SosefThe section Loasibegonia now comprises 19 species, 10 subspecies and 2 varieties. The section Scutobegonia has 21 species and 2 varieties