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African Fig Trees and Fig Wasps

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African Fig Trees and Fig Wasps African tig trees and tig wasps Koninklijke Nederlandse Akademie van Wetenschappen Verhandelingen Afdeling Natuurkunde, Tweede Reeks, Deel 89 African fig trees and fig wasps C.C. BERG AND J.T. WIEBES North-Holland, AmsterdamlOxford/New YorklTokyo, 1992 C.C. BERG The Norwegian Arboretum, N-5067 Store Milde, Norway l .T . WIEBES Florijn 13, 2353 TC Leiderdorp, The Netherlands ISBN 0-444-85741-9 Contents I. Introduction 7 Referenee 8 11. Biology of figs and fig wasps Introduetion 9 The development of the figs 9 The habits of fig trees II The leaves l3 Stipules and buds 14 The position and size of the figs 14 The strueture of the fig 15 The flowers 17 The staminate flowers 18 The pistillate flowers 19 The pollinators 22 Colonization of the syeonia 24 Oviposition and pollination 25 Eclosion from the galls and mating of the was ps 26 Eclosion from the syeonium 28 The number of otTspring and the sex-ratio of the wasps 28 Phenology 28 The infrueteseenee and the fruitlets 30 Dispersal 31 Germination 31 Hybridization 32 The classifieation of the figs 33 The classifieation of the pollinators 36 Comparison of the classifieations of figs and wasps 37 The origin and development of the symbiosis 39 Parasitoids and predators 41 References 43 In. The genus Ficus in Afriea Introduction 47 Taxonomie history 47 Distribution 48 Diagnosis of the genus Ficus L. 51 Keys to the sections 51 Keys to the species 52 African groups and species 62 Introduced species 166 Reference 167 IV. The African fig wasps Introduction 169 Key to the genera 170 African groups and species 173 References 192 V. The poUinators (Agaoninae) Diagnosis 195 Introduced species 195 Classitication 196 Key to the genera 196 African genera and species 200 References 273 VI. Bibliography 275 VII. Index Scientitic names of animals (and Bacteria) 287 Scientitic tig names 291 I. Introduction The present publication is the result of a long-standing co-operation between the authors, Berg studying the taxonomy of Ficus and Wiebes describing the insects that could be reared from the figs. The explicit understanding was from the beginning, that the botanica I and entomological taxonomic studies would be independent. These activities led to a number of papers on the figs and fig wasps of the African region (including Madagascar), resulting in the check-lists of Ficus (Berg, 1990c) and the Agaonidae (Wiebes & Compton, 1990). The co-operation was considerably intensified and broadened by the par­ ticipation in a french CNRS-Écotrop-programme (see e.g., Lachaise, 1984), which also involved other biologists studying other groups of fig-symbionts and their biology. High-lights of our concerted efforts (not mentioning many indi­ vidual trips, mainly by Berg) certainly were the collecting trip that the authors made into Ivory Coast (1982), together with Dr. G. Michaloud, and the sym­ posiums in Paris (1983) and Montpellier (1984). Two grants from the dutch ZWO-BION, the first one allowing Dr. S.A. UIen berg to study a genus of fig­ wasp-parasitoids, i.e., Apocrypta (UIenberg, 1982- 1985), and a second one to Dr. W. Verkerke, for a study of the fig-morphology (Verkerke, 1986-1990), substantially supported our study. Gradually, the knowledge of African figs and fig was ps attained a level at which the publication of a synopsis has become desirabIe, if only to show the state of our present knowledge to other students of the fig-symbiosis, and to all ow them to identify the figs and wasps that they find. The plan of tbis book is as follows. In four consecutive chapters the various aspects of figs and fig-wasps are treated, folio wed by a bibliography of African figs and fig wasps. The references that are not included in the bibliography, because they do not pertain to Africa, are given in a paragraph of references, after each cha pter. Our activities, and especially the participation in the Écotrop-program, pro­ moted contacts with many other students of figs and fig-insects. To all, we are greatly indebted for their collaboration and friendsbip, which we value very much: Getachew Aweke (Addis Ababa), Himansu Baijnath (Durban), Mike Bingham (Lusaka), Steve Compton (Grahamstown), Ib Friis (Copenhagen), Jacob Galil (Tel-Aviv), Veldie van Greuning (Pretoria), Finn Kjellberg (Mont­ pellier), Daniel Lachaise (Gif-sur-Yvette), Géorges (and the late Sylvie) Micha­ loud (Montpellier), Tom Müller (Harare), Anders Nilsson and Börge Pettersson 7 (Uppsala), Simon van Noort (Grahamstown), Shamilla Ramcharun (Durban), Sandrine UIenberg (Amsterdam), Géorges Valdeyron (Montpellier), Wouter Verkerke (fonnerly in Amsterdam), Anthony Watsham (Harare). The provenance of the figures, most of which were published before, is ac­ knowledged in the captions. Some of the entomological drawings were borrowed from publications by Guido Grandi and one or two by Zdenek Boucek, Jacob Galil, and Anthony Watsham, but most were made by Wiebes. For the botanical drawings, and for the kind pennission to use them in the present publication, thanks are due to E Croizier and D. Molez, Laboratoire de Phanérogamie, Muséum National d'Histoire Naturelle, Paris; EM. Bata-Gillot, E. Jens, J. Wil­ liamson and I. Zewald, Department of Plant Taxonomy and Geography, Agri­ cultural University of Wageningen; E.M. Hupkens van der EIst and T. Schipper, Institute for Systematic Botany, University of Utrecht; W. Verkerke, Hugo de Vries Laboratory, University of Amsterdam; S. Dawson, Royal Botanic Gar­ dens, Kew. S. Herland, of the Botanical Institute, University of Bergen, adapted some of the drawings to our present requisite. Dr. S. Edwards, of the Manchester Museum (U.K.), is thanked for making available the coloured plate of the cover, showing Ficus sansibarica subspecies macrosperma in full fruit. REFERENCE Lachaise, D. (ed.) - Programme Écotrop. Interface plantes-insectes en milieu tropical: relations entre les stratégies adaptives des figuiers et celles des insectes des figues. Courrier de I'Écotrop, Numéro spécial, 1...{j9 (avril 1984). 8 II. Biology of figs and fig wasps Introduction Figs (Ficus L.) and the pollinating tig-insects (Agaoninae) form an unbreakable unity. It is true th at individual tig trees can grow, but for their propagation pollinators are indispensable. Outside the tig inflorescence, the pollinators live only for at most a few days. Ficus is the only genus of the tribe Ficeae, one of the tive recognized in the family Moraceae (Berg, 1989b). Because of its urceolate inflorescence, the genus Sparattosyce has been regarded as related to Ficus, but such inflorescences ap­ pear to occur also in other genera of the Moraceae and even in the Urticaceae. Both the tri bes Ficeae and Dorstenieae are characterized by a general occurrence of (basically) bisexual inflorescences. The Ficeae cannot readily be related with any other tribe of the Moraceae, which may imply that Ficus represents an early branch-off in the history of the Moraceae. The pollinators form the subfamily Agaoninae of the Hymenoptera Chalcidoidea. They have some resemblance to the Sycoecinae (see Chapter IV) which, however, is based on the very instru­ ments used for entering the tig, and thus may result from a parallel development. The wing-venation is distinctiy different. The males of the Agaoninae are wing­ less, they are winged in the Sycoecinae. Also the tig-pollinators appear to form an old group. In a recent review, Berg (1990a) treated the botanical aspects of the symbiosis of tigs and wasps; some years earlier, Wiebes (1986a) had discussed general features from the entomological point of view. Among older reviews are Janzen (1979) and Wiebes (1977a, 1979c). In 1988, a research colloquium under the auspices of the american NSF and the french CNRS, brought together in Miarni a number of botanists and entomologists interested in the tig-wasp-mutualism (multi-author review, see references under Miarni). In a nurnber of paragraphs, some morphological and biological features interesting to our purpose, will be discussed below, to begin with the two peculiar features of tigs, viz., the develop­ ment of the tigs and the pollination of their flowers by tig wasps, and the hemi­ epiphytic life-habit of many of the tig-species. The development of the figs The fruit-like inflorescence of Ficus - tig or syconium - consists of a more or less globular (or urn-shaped) hollow receptacle, fully enclosing the flowers borne 9 --'II,..,JJc:---- 0 S T lOL E b c Fig. I. Anatomy of a fig-sycone, and of staminate (a) and pistillate flowers (b, short-, and c, long­ styled flower). After Wiebes (1982a, fig. I). on the inner side (fig. I). There are three main types of flowers, viz., staminate flowers (fig. Ia) and pistillate flowers, divided into long-styled flowers ('seed­ flowers', fig. Ic) and short-styled flowers ('gall-flowers', fig. I b). If the two types of pistillate flowers, together with the staminate flowers, occur in one and the same syconium (as in the monoecious species), intermedia te style-Iengths are found and all pistillate flowers can produce seed (Neeman & Galil, 1978). If the two types of pistillate flowers occur in different figs (as in the gynodioecious species), intermediate style-Iengths are not found and usuallly only the long­ styled flowers produce seed. In gynodioecious species the short-styled flowers occur together with staminate flowers in 'gall figs' , while figs containing the long-styled flowers ('seed figs') lack staminate flowers. The two types of fig are found on different trees. A survey of features connected with monoecy and gyno-dioecy in Ficus is presented in table I. Most of the African species of Ficus are monoecious, only Ficus pa/mala and the species of section Sycidium (together 10 out of 105 African species) are gynodioecious. In the development of the syconium Galil & Eisikowitch (l968c) distinguished between a number of phases, as follows (fig.
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