BS 55 423 diversity in a global perspective

Cornelis C. Berg

Berg, C.C. 2005. Moraceae diversity in a global perspective. Biol. Skr. 55: 423-440. ISSN 0366-3612. ISBN 87-7304-304-4.

The Moraceae are tightly embedded in the Urticales, a clear-cut entity of the Angiospermae. It comprises c. 1050 species and 37 genera, many of which have 1 or 2 species, and a few are large: has nearly 750 spp., has c. 105 spp., and has c. 60 spp. The family is pantropical, with extensions to subtropical and warm-temperate regions. It is well-represented in all tropical phytogeographic regions, each with one or more primary and/or secondary centres of distribution. The family is very diverse in both woody and herbaceous life and growth forms, but even more so in reproductive structures, comprising by condensation and fusion complex inflorescences, of which some are pseudoflorous and others are pseudocarpous, such as those of Ficus in which stigmas and anthers are not exposed at anthesis. This is linked to an unique polli­ nation system. For other Moraceae pollination is by wind and adapted to forest conditions, or they are pollinated by small beetles, flies, or thrips and based on breeding in staminate inflores­ cences, or the mode of pollination is unknown. Patterns of Moraceae diversification, its func­ tional implications, patterns of distribution, and the distinctness of genera and tribes suggest that most of the differentiation of the family took place in a still coherent tropical continent. The dis­ tinctness of taxa is not reflected in cladograms based on molecular analyses; one may wonder why.

Cornelis C. Berg, The Norwegian Arboretum/Botanical Institute, University of Bergen, 5259 Hjellestad, Nor­ way. E-mail: [email protected]. - National Herbarium Nederland, Univ. Leiden branch, P.O. Box 9514, 2300 RA Leiden, The Netherlands. E-mail: [email protected]

Introduction Urticales This paper summarizes various previously pub­ Except for doubt about the position of some lished aspects of the diversity and distribution odd genera or families (e.g, Barbeyaceae), the of Moraceae (Berg 1977a, 1983, 1989, 1990, Urticales was soon recognized and generally 1998, 2001) and discusses the overall taxo­ accepted as a well-defined group in the process nomic structure of the family and how they are of defining “natural” entities, as by Bentham linked to patterns of morphological and bio­ (1880), Bailion (1875), Eichler (1875), Engler logical diversification and distribution. Finally, (1889). The solidity of the order is in recent these morphological and biological aspects are times confirmed, e.g., by Baas et al. (2000) who compared with results of molecular analyses considered the wood anatomy as well as by (Sytsma et al. 2002). results of molecular analyses (Sytsma et al. 2002). 424 BS 55

The position of the order within the ply of food to frugivorous animals (Balslev & angiosperms has been uncertain. Traditionally Renner 1989; Gentry 1993; Berg 1998; Shana­ it is linked to the amentiferous families, han et al. 2001). grouped in the Hamamelidae (Cronquist 1981). A position near the Malvales (and Euphorbiaceae) has been advocated (Berg Composition of the family 1989). Molecular studies indicate a link to the The genera are very unequal in species num­ (c.g., Sytsma et al. 2002) and the order bers; 13 genera have only one or two closely is then referred to as Urticalean . Roses related species; 14 genera have three to 14 and nettles in the same taxonomic unit are, species; few have more, and although they share the capacity to sting, diffi­ 20-25 species, Artocarpus c. 60 species, Dorstenia cult to accept for morphological reasons. c. 105 species, and Ficus nearly 750 species and, therewith, one of the largest genera of woody flowering . Moraceae The Moraceae can be regarded as a “natural entity”, after exclusion of the genera in the Habit subfamilies Conocephaloideae and the The family is predominantly woody. The two Cannaboideae in Engler’s classification, the species of Fatoua are herbaceous. Eleven former being included in the Cecropiaceae species of Dorstenia are woody, the others are (Berg 1989) and the latter in the Cannabaceae herbaceous and represent a wide range of life (Cronquist 1981). and growth forms (Berg 1977a; Berg & Hijman In its morphological differentiation, the 1999; Fig. 2). family shows strong links to the other larger The woody Moraceae vary from being small urticalean families currently recognized. These shrubs to tall trees with sympodial or monopo­ links are such that one could unite Moraceae, dial growth. Few species are (sub) monocaul, Cecropiaceae, and Urticaceae into a single Dorstenia djettii], L. Guillaumet, Naucleopsis stip­ family. If one is not too narrow-minded, even ularis Ducke, and some Ficus species, e.g., F. Ulmaceae (both Celtidoideae and Ulmoideae) pseudopalma Blanco. Several Ficus species are can be included in this more broadly con­ rheophytic (van Steenis 1981). strued family Urticaceae, thus, largely coincid­ The capacity of Ficus to produce aerial ing with the order Urticales. adventitious roots, contributes considerably to However, such a broadly construed family the diversity of the woody life and growth lacks the transparency one needs to analyse forms, as hemi-epiphytes, hemi-epiliths, and morphological differentiation and distribution root-climbers. patterns in relation to biological traits and evo­ The plants have a system of ducts extending lutionary processes leading to its present taxo­ from the stem to the leaves and containing nomic structure. In this respect, it is conve­ milksap (not in Fatoua). Uncinate hairs occur nient to maintain a family Moraceae and its in many genera, and pluricellular (“glandu­ presumably natural subdivisions (Fig. 1). lar”) trichomes in most (or all?) genera. Nearly Compared to many other tropical fam­ all Ficus species have waxy glandular spots on ilies, the Moraceae is with its 1050-1100 species the lamina, base of the petiole and/or nodes of small, but in many tropical lowlands it is ecoli- leafy twigs. cally and important in forest structure and sup­ The height of the plants varies from less than BS 55 425

Fig. 1. Distribution and sub­ America Africa Asia Australasia division of Moraceae. The (ca 70) (11) (12) (c 47) survey gives the representa­ Madura (3*) Madura (1) Madura (7) tion in the three main phy­ (3*) Morus (1) Morus (c 8) togeographic regions and (5) Trophis (2) Trophis (2) tribes with the numbers of Bleekrodea (1) Bleekrodea (1) species () per genus tribe, (1) Broussonetia (7) and region; in Ficus (Ficeae) Fatoua (1) Fatoua (1) per subgenus (for the Streblus (3) Streblus (21) entirely or mainly Milicia (2) Artocarpeae (c 70) (c 68) (gyno) dioecious subgenera (3) (3) (B) or for the (main) sec­ Artocarpus (c 60) tions of the monoecious Hullettia (2) subgenera (A) Ficus = (2) Ficeae), and the indigenous Prainea (4) genera in [ ]; * including a Soroceae (23) (23) species in North America; o (1) all (gyno) dioecious. Africa (3) includes Madagascar, adja­ (3) cent Indian Ocean Islands, (2) and the Arabian Peninsula (14) with adjacent islands. "Antiariopsidae" (3 (3) (2) Sparattosyce ( 1 ) Dorstenieae (128) (64) (63) (1) Dorste nia (46) Dorstenia (58) Dorstenia (1) Bosqueiopsis ( 1 ) (2) (1) Utsetela (1) (14) Helianthostylis (2) Trymatococcus (2) Castilleae (58) (55) (2) (1) (1) Antiaris (1) (1) (3) (7) (4) Naudeopsis (22) (9) (10) Ficeae (c.735) (c 120) (105) (c 510) "A" (c 350) (c 120) (83) (c 150) Pharmacosycea (c 20) Oreosycea (4) Oreosycea (c 50) Americana (c 100) Urostigma (7) Urostigma (c 80) Galoglychia (72) Stilpnophyllum (c 20) "B" (c 360) (22) (c 360) Ficus (1) Ficus (c 60) Synoecia (c 80) Sycidium (9) Sycidium (c 100) Sycomorus (12v) Sycomorus (c 120) 19[14] gen (c 270) 17[7]gen (185) 16[6] gen (c 610) 426 BS 55

WOODY PLANTS ------> Herbaceous plants(1)

TERRESTRIAL--- > Hemi-epiphytic(2) --- > Hemi-epilithic(2)

TREES ------> Shrubs (3) --- > ------> Cli mb e r s ( 4 )-- ►

Small Medium-sized (rarely with thorns or prickles) Emergents

—► Climbers > Shrubs------► Rheophytic (5) Straggling(6) Obligatory With roots(7) Facultative With thorns(8) Erect ------> Holo-epiphytic(9 Creeping (10)

Herbaceous plants

TERRESTRIAL------► Holo-epiphytic ( 11 )

PERRENIAL ------► Annual(12)

NON-SUCCULENT ------► Succulent(13) Stem-succulent Tuber-succulent (geophytic or not)

Phanerophytic (14) Geophytic(15) Erect Stem normal Not rosulate* Stem tuberous Rosulate* Creeping *Internodes long versus short Fig. 2. Life and habit forms of Moraceae. The numbers indicate that the life and habit forms are represented in the fol­ lowing genera and species: (1) Dorstenia p.maj.p. (2) Heus p.p. (3) Bleekrodea, Brosmium p.p., Ficus p.p., Helianthostylis p.p., Perebea p.p., Scyphosyce, Soroceap.p., Utsetlea. (4) Broussonetia kurzii, Ficus p.p., Madura p.maj.p., Prainea scandens, Trophis scan­ dens. (5) Ficus p.p. (6) Broussonetia kurzii, Ficus p.p., Prainea scandens, Trophis scandens. (7) Ficus p.p. (8) Madura p.p. (9) Ficus deltoidea (and F. oleifolid), facultatively. (10) Ficus p.p. (11) Dorstenia astyanactis. (12) Dorstenia annua. (13) Dorstenia p.p., Fatoua. (14) Dorstenia p.p.

5 cm as in some creeping Dorstenia species C.C. Berg (Berg 1972), or possibly even taller (Berg 2001) to 50 in tall, as in Brosimum utile in some Ficus species. (Kunth) Pittier and Maquira coriacea (Karst.) BS 55 427

Leaves Inflorescences

The basic type of leaf has a short petiole and a The inflorescences are mostly condensed basally attached, coriaceous, elliptic lamina (unbranched) with similar parts (flowers) and with entire margin, pinnnate to subtriplin- dissimilar parts (flowers, bracts, and/or recep­ erved brochidodromous venation with scalari- tacles) often fused, resulting in structures form tertiary venation; the stipules are often which function as units of pollination, resem­ fully amplexicaul, leaving the characteristic bling either flowers, thus pseudoflorous, or annular scars. Most of the variation in these fruits, thus pseudocarpous (Berg 1977a, 1989). features can be linked to life form or habitat. Much of the differentiation of the inflores­ cences (and flowers) can be related to protec­ tion of developing stamens, pistils and fruits, Sexuality which is essential for pollination based on Like in other Urticales families (with the breeding in staminate inflorescences (Berg notable exception of Cecropiaceae), monoecy 1990). (with either bisexual inflorescences or unisex­ Most of the least condensed inflorescences ual inflorescences) and dioecy are about (as racemes and cymes) are found in equally represented. Bisexual inflorescences anemophilous taxa in which the staminate are mainly found in groups with cymose inflo- flowers need space for ballistic pollen release; resences and unisexual ones in racemous ones. the pistillate inflorescences of these taxa are Androdioecy is rare, it is found in Castilla elas­ often more condensed, but the flowers usually tica (Sakai 2001) and Helianthostylis sprucei remain free. (Berg 1972). Gynodioecy is found in Ficus, in The abaxial sterile strip commonly found in which in c. 50% of the species the plants bear elongate inflorescences is caused by the basi­ inflorescences with only long-styled pistillate cally adaxial orientation of the flowers. flowers or with staminate flowers and short- The most complex and intricate inflores­ styled pistillate ones, which, however, normally cence of the Moraceae (and angiosperms?) is do not produce seeds. Gynodioecy or androdi­ that of Trilepisium (Berg 1977b: 298, t. 6 and 7). oecy may also occur in some (other) species of The inflorescences occur basically in pairs in Castilleae in which pistillate and staminate the leaf axils. In some groups, e.g., in Castilleae inflorescences occur on the same tree, whereas and in Ficus (e.g., in subg. Urostigma'), inflores­ others only bear pistillate or staminate ones; it cences develope on axillary spurs (which may is not clear whether differences in distribution continue to elongate on the older wood) that of sexes in this tribe is related to age. For some often bear more than two inflorescences simul­ species switch of sexuality is known: Dorstenia taneously, in some Castilleae even several sta­ cayapya Veil, produces first staminate, later pis­ minate inflorescences and a single pistillate tillate inflorescences, and Brosimum alicastrum one. Cauliflory is found in Artocarpus, Clarisia, Sw. first produces predominantly pistillate Treculia and in some subdivisions of Ficus', subg. inflorescences then predominantly staminate Urostigma (sect. Galoglychia), subg. Sycidium, ones (see Berg 2001 ). Changes in sexuality may subg. Sycomorus, and subg. Synoecia; in subg. also occur in Castilleae species of which some Sycomorus, many species are or can be flagel- of the trees bear both staminate and pistillate liflorous (or geocarpic). inflorescences. 428 BS 55

Flowers a hard endocarp) enclosed by the fleshy fruit­ ing perianth. Pseudodrupes may occur free or The flowers are small. Through reduction in fused in (syncarpous) aggregates. The more size and numbers and through fusion of simi­ complex fruit-containing structures show simi­ lar or dissimilar parts a wide range of Hower larities to the “infructescence” of the pineap­ types have developed from the basically (3-)4(- ple. 5)-merous, monochlamydous, unisexual Dehiscent drupes, or indehiscent ones with flower, the pistillate one with a single (sub) api­ features deary derived from the dehiscent cal ovule and two stigmas (Berg 1977a, 1989) ones are found throughout the family (Berg and the staminate one with antitepalous sta­ 1977a), even in Ficus (Berg & Wiebes 1992). mens and often without pistillode. The peri­ The endocarp body is squeezed out of the fruit anth may become rudimentary or absent, and in macrospermous species, but it is ejected in the number of stamens reduced to one. A sin­ microspermous ones (Dorstenia p.p. and gle stigma is quite common. Pistillodes are pre­ Fatoud). sent in all species with ballistic pollen release, In many-seeded infructescences of Dorstenia, as they seem to play a role in keeping the each single fruit (dehiscent drupe!) remains inflexed anthers under tension and in the cor­ the unit of dispersal. This may also be the case rect position. Pistillodes are charactersitic for in Ficus, depending on the “disperser” (a “seed­ Ficus subg. Sycidium, where they are in some eater” rather than a “fruit-eater”). species so large that they can function as breed­ The units of dispersal vary from fruits or ing sites for fig wasps. Pistillodes with very long pyrenes of c. 2 mm length to syncarpous stigmas occur in Helianthostylis sprucei Baill. infructescences up to 100 x 50 cm in Artocarpus (Berg 1972). heterophyllusL^m. (Jarrett 1959-1960). In the species of the Moreae, with the excep­ The fleshy fruits, pseudodrupes or infructes­ tion of some Asian Madura species, the sta­ cences vary in colour from green to yellow, mens are like those of the Urticaceae, releasing orange, brown, red, purple or black (or white). the pollen suddenly. They differ from inflexed stamens of other Urticales in showing trans­ verse (tension) lines on straightened filaments Seeds The differentiation of the flowers is tightly The seeds are very variable in the size, the pres­ linked to the (degree of) complexity of the ence of endosperm, the texture of testa, the inflorescence and to protection of young flow­ position/orientation of the seed in the fruit, ers and developing fruits (Berg 1990). the thickness, folding, and size (differences) of the cotyledons, and the length and position of the radicle (Corner 1962). Fruits and “fruits” The majority of the genera are macrosper­ In addition to the “true” fruits (developed mous; the seed lack (ample) endosperm and from a single ovary and being achenes or dru­ the cotyledons are thick, often folded, and/or pes (indehiscent or dehiscent!), there is a wide unequal in size, conspicuously so in Sorocea, range of “functional fruits”, containing one or which is submonocotyledonous. Microsper­ more seeds, and also consisting of perianths, mous seeds are found in Ficus, the c. 95 herba­ bracts and/or receptacle, that usually function ceous species Dorstenia, and several genera of as units of dispersal. The most simple ones the Moreae; the seed contains endosperm and (“pseudodrupes”) consist of a fruit (often with the equal cotyledons are thin. Macrospermy is BS 55 429 linked to the rain forest habitat; microspermy are nutritious (providing a substrate for fungi) is related to the herbaceous habit, hemiepi- pollination may be carried out by collecting phytism, and occurrence of secondary growth. the trichomes (Berg 1990, 2001). The protective function of the testa is trans­ In several genera, in particular those with ferred to the woody to leathery endocarp/peri- bisexual inflorescences of the Dorstenieae carp; the testa is usually distinctly vascularized. nothing is known about pollination and fea­ tures of flowers and inflorescences do not point to possible modes of pollination other Pollination than (geitonogamous) autogamy. Agamo­ The following modes of pollination are found. spermy may play a role in reproduction of Anemophily. (1) with sudden ballistic pollen Dorstenia (Berg & Hijman 1999). release (in most Moreae) or (2) with ± gradual pollen release, e.g., from long pendulous stami­ nate “catkins” (possibly in Bagassa, Batocarpus, Dispersal Clarisia p.p., and reported for some species of The following modes of dispersal are known. Artocarpus without elongate staminate inflores­ Endozoochory in taxa with fleshy (true or cences) . The first type, characteristic for functional) fruits: (1) by arboreous animals Urticaceae, can be regarded as an adaptation (majority), (2) by terrestrial animals {Artocar­ to the rain forest understorey, in particular pus, Ficus, and Treculia with cauliflory or flagel- along small streams, where streaming water liflory), or (3) by aquatic animals {e.g., Ficus in may cause (weak) air current by which pollen riverine habitats). is carried. Exozoochory. (1) in taxa with fruits with a Zoophily. (1) based on breeding in develop­ sticky outer layer {Ficus) or (2) in Trymatococcus ing fruits by the small Agaoninae wasps {Ficus) of which the infructescences are covered with or (2) based on breeding in staminate inflores­ hooked hairs. cences by small beetles and flies. The latter Fruits of Ficus deposited (by endo- or exo- mode is reported for some Artocarpus species, chorous transport) on tree branches, may be but probably widespread, to be found in gen­ carried on by ants (to more suitable germina­ era with condensed staminate inflorescences tion sites). (as those of Castilleae and Artocarpeae) ; insect Autochory in most taxa with dehiscent dru­ larvae are nearly always present in these inflo­ pes, the endocarps of small ones are ejected, rescences. those of large ones dropped, and both trans­ Moreover, Sakai et al. (2000) described polli­ ported further by water. nation in Artocarpus integer (Thunb.) Merr., car­ Hydrochorous in some Ficus species of which ried out by gall midges, of which larvae feed on the syconia can float, either by air inside the mycelium growing on staminate inflores­ infructescence or by a spongy wall of the inflo­ cences; it is not clear whether the situation rescence. The rheophytic species of Ficus described is a local or a general phenomenon. (subg. Sycomorus subsect. Macrostyla) have Pollination by thrips is found in Castilla elastica retrorse hairs on the (very) long persistent Sessé (Sakai 2001). The racemose or spicate style and on the fruit, apparently an adaptation inflorescences of Sorocea resemble those of gen­ to attach the fruits to the substrate. era with ballistic pollen release (Moreae), but The in general species-specific relations with the stamens are short. As the perianths of pis­ pollinators limit the possibilities of long-dis­ tillate flowers bear glandular trichomes which tance establishment of populations. 430 BS 55 BS 55 431

Tribal ceae, Artocarpeae, and “Antiaropsideae” (inedi), respectively. There might be a phyloge­ The family comprises 1050-1100 species, netic link between the “Antiaropsideae” and accommodated in 37 genera, which as cur­ Ficeae. rently defined (see Fig. 1) can be regarded as The distribution patterns and the lack of natural (or monophyletic) entities. clear affinities between the tribes suggest that Until recently (Berg 2001) five tribes were the family was established and the genera to a recognized: largely shaped before the break-up of Artocarpeae with 12 genera and 90-95 Gondawana, an opinion (Berg 1998) which is species, Castilleae with eight genera and c. 60 confirmed by research on Ficus (Molbo et al. species, Dorstenieae with eight genera and c. 2003; Weiblen 2002). 130 species, Ficeae with one genus and c. 720 The distinctness of the tribes is not only species, and Moreae with eight genera and c. defined by their morphological make-up, but 70 species. All, except for the Artocarpeae are also by biological traits as expressed in the well-defined and can be regarded as natural mode of pollination and habitat occupation. entities. The Artocarpeae comprise the genera that could not be satifactorily included in one of the other tribes. They comprise a group of Taxonomy of Ficus five neotropical genera (with 23 species), a Ficus is not only far more numerous than the group of four Asian genera (Artocarpus and other genera, but is also morphologically dis­ three allied Asian genera) and the African Tre- tinct in characters not found in other culia (in total with c. 65-70 species), and a Moraceae, many of them related to the unique group comprising two genera: Antiaropsis with pollination system. Moreover, the systematic two species from New Guinea, and the mono­ make-up tells the genus apart. typic Sparattosyce from New Caledonia (Fig. 3). The unique pollination system is based on The neotropical group of genera resembles breeding in ovaries by Agaoninae (c 20 genera, the Moreae in shape and structure of the inflo­ numerous species, roughly as many as the rescences, but is clearly different in the struc­ number of Ficus species) of which the winged ture of the staminate flowers. The small group females transport pollen, penetrate the closed formed by Antiaropsis and Sparattosyce resem­ inflorescence, lay eggs in the ovules, and bles the Castilleae in the shape and structure deposit pollen. The pollination system is in its of the inflorescences, but differs clearly in the basic traits uniform, but in details highly varied presence of dehiscent drupes and scarious due to the pollinator groups involved and the tepals of the pistillate flowers. The morpholog­ variation of characters of flowers and inflores­ ical links between these three groups are as cence. weak as between the “natural tribes” and can, Gharacters that distinguish Ficus from other therefore, be regarded as tribes equivalent to Moraceae are: the other four tribes and to be named Soro- (1) . The flowers remain entirely enclosed in

Fig. 3. Sparattosyce dioica, from Ann. Sei. Nat. Bot., Sér. 5, 11: t. 6 (1869): 1 and 2. Staminate inflorescences, closed; 3 and 4. staminate inflorescences, open; 5 and 6. staminate flowers; 7 tepal of staminate flower; 8 and 9. stamens; 10, 14, and 15. pis­ tillate inflorescence, closed; 11. pistillate flower; 12. pistil; 13 and 16. ovary; 17. fruit; 18. embryo. The pistillate inflores­ cence opens like the staminate one to expose the ripe fruits and to release the endocarp bodies of the dehiscent drupes. 432 BS 55 an urceolate receptacle (syconium) also dur­ the apical opening and the receptacle splits to ing anthesis. expose the dehiscent drupes; the staminate (2) . Heterostyly (imperfect or perfect); the ones opens in the same way to expose the sta­ stigmas lined up (in monoecious taxa due to mens at anthesis. differences in the length of the pedicel (or also The stibgenera of Ficus are in their numbers the shape of the ovary). of species similar to several moraceous tribes. (3) . Pedicels of pistillate flowers distinctly These numbers and the diversification within different in length in the same inflorescence. the genus makes it appear the genus is like “a (4) . The number of staminate flowers (per family within a family” (Corner 1958), with a inflorescence or per plant) is mostly (very) diversity that equals that of many large small in relation to the number of pistillate angiosperm families; subsections and sections flowers. currently recognised are more or less clearly (5) . Scarious tepals of the pistillate flowers. equivalent to genera and subgenera to tribes. (6) . Formation of a coherent layer of stig­ Far ahead of modern developments the Italian mata (synstigma) in spite of style lengths in the botanist Gasparrini (1844, 1845) started to same syconium. split Ficus into new genera largely based on flo­ (7) . Waxy glandular spots on the lamina ral characters. This concept was adopted by the beneath and/or the nodes of leafy twigs in great Dutch “ficologist” Miquel (1847-1848), nearly all species. who expanded the number of genera, but Other differentiating characters: finally he met the limits of the possibilities for (8) . Pronounced protogyny: the staminate systematization and had to include all those flowers are at anthesis when in the same inflo­ about 20 genera in Ficus (Miquel 1867). Many rescence the seeds are (nearly) ripe. of those genera became subdivisions of the (9) . The perianth (and interfloral bracts genus. The more recent and elaborate classifi­ and/or internal hairs) remained intact in spite cation of the genus by Corner (1960, 1965) of loss of the(ir) protective function. includes c. 125 entities: subgenera, sections, In addition to these largely floral characters, subsections, series, and subseries - too many Ficus differs from the rest of the Moraceae by trees to see the forest. A more concise classifi­ the numerous species (c 390) that produce aer­ cation is proposed (Berg 2003) of which out­ ial roots, and for most of them (c 290) allowing lines are presented in Fig. 1. them to be hemi-epiphytes and others to be The morphological and ecological differen­ root-climbers (c 70). Moreover, in (the monoe­ tiation within the genus, the distribution pat­ cious subgenera) Ficus, the tertiary venation of terns (Fig. 4, 5 & 8), the biological distinctness, the lamina can be parallel to the lateral veins. the diversification in the pollination system as The only moraceous genus with inflores­ reflected in the number of genera of pollinat­ cences resembling of Ficus is Sparattosyce (Fig. ing wasps and other groups of insects exploit­ 3), but the inflorescences are unisexual, the ing the system, and the differences with the pistillate ones exposing the stigmas through “other” Moraceae suggest that Ficus established

Fig. 4 . Distribution of three subgenera and sections of Ficus with the numbers of species for each. Continuous lines for the —> primary centres, broken lines for secondary ones; lines and arrows for main distribution tracks; G for groups of species associated with humid conditions, G’ for groups of species associated with drier conditions; U for subsect. Conosycea, asso­ ciated with humid conditions, U’ for subsect. Urostigma, associated with drier regions. BS 55 433 434 BS 55 itself as distinct group early in the history of nently by ostiolar bracts, in Castilleae and the Urticales (Molbo et al. 2003; Weiblen “Antiaropsideae” temporarily by the upper 2002). Also wood-anatomical features support involucral bracts, in the former tribe to stami­ the fairly isolated position of the genus (Koek- nate flowers and pistillate flowers in unisexual Noorman et al. 1984). inflorescences, in the latter also pistillate ones with more than one pistillate flower. However, Trophis caucana (Pittier) C.C. Berg, which Molecular phylogeny of Ficus and belongs to the tribe Moreae, also has involu­ Moreae cres of imbricate bracts; in the genus the bracts It is surprising that molecular data as pre­ are basally attached and also uncinate hairs sented by Systsma et al. (2002) do not support absent. the profound distinctness of Ficus (Ficeae). It Another result of the same molecular analy­ ends up in a cluster together with the tribe ses (Sytsma et al. 2002) that is clearly in conflict Castilleae, one would never consider to be with a traditional concept, is the scattered related because of fundamental differences in occurrence of members of the Moreae which the structure and function of the inflores­ appears on the basis of morphological coher­ cence. However, the Castilleae and Ficus share ence and distribution to be such a nice natural the absence of some characters, such as the group. It also raises the question how often the absence of peltate bracts and, if one ignores urticaceous type of androecium (staminate the presence in three unrelated species of Ficus flower) can evolve or disappear without leaving (F asperiuscula Kunth & C.D. Bouché of subg. any trace of an ancestral trait. Sycidium, F. recurva Blume of subg. Synoecia, and F. theophrastoides Seem, of subg. Sycomorus) also the absence of uncinate hairs. If these charac­ Molecular phylogeny of Urticales ters express affinities, then one could predict Another case in this publication that does not that also Antiaropsis and Sparattosyce (“Antiarop- reflect distinctness and presumably different sideae”) will end up in the same cluster. evolutionary pathways is the presence of the The indumentum character do not appear neotropical lowland genus Ampelocera, that biologically important, and is in that respect, one could indicate as the most tropical of the similar to macro- and micromorphological Ulmaceae, in a cluster of genera which share characters which are mostly used in the cited abscission of the terminal meristems, a feature paper presenting the results of molecular also found in the moraceous genera Brous- analyses to explain clustering of taxa. The sonetia ands Morus, and in Tilia (Tiliaceae). bracts character, may have more than subordi­ This feature links these genera (of which rep­ nate, although somewhat ambiguous biological resentatives may secondarily occur in the low­ importance, if one assumes that basal attach­ land tropics) to development under northern ment of bracts is a prerequisite for the estab­ temperate conditions. The presence of a tiny lishment of rows of imbricate bracts with may hypanthum, although it is the most rosaceous close off access to the flowers, in Ficus perma­ character in the Urticales, but probably with lit-

Fig. 5 . Distribution of three subgenera of Ficus with the numbers of species for each. Continuous lines for the primary cen­ tres, broken lines for secondary ones; lines and arrows for main distribution tracks; S for sect. Sycomorus subsect. Sycomorous with only monoecious species. BS 55 435 436 BS 55 tie biological significance, is indicated as one important is that the group is biologically so the unifying morphological characters. The different in the absence (loss?) of urticaceous other character, bisexuality of the flowers, is stamens and it is, therewith, not not consistent and also found in other anemophilous. Characters such as condensed Ulmaceae. inflorescences, fleshy staminate perianths, A similar case is the position of the five large protective stipules (and spathes) can be clearly related (We st-Go nd wan an) genera of linked to disconnection from anemophily (if the Cecropiaceae. They differ from Urticaceae that would have been an ancestral trait at all). in a good number of macromorphological, Adaptations to (secondary?) anemophily as in chemical and microscopic characters. More Cecropia are highly peculiar and diverse. Do the

Fig. 6. Distribution of four tribes of Moraceae, with the numbers of species for each. Continuous lines for primary centres, broken lines for secondary ones. Thick broken lines for strong links between partial areas. Continuous and broken lines and arrows for main distribution tracks. Small circle for Artocarpeae in Africa for Treculia. BS 55 437 molecular bases of to characters like presence tropical or even warm-temperate zones (Fig. of arachnoid indumentum and pearl glands 8). Broussonetia and Morus are clearly associated make that the btdk of the Cecropiaceae to clus­ with the northern warm-temperate zone. They ter with the Boehmerieae? are morphologically adapted to nontropical climates through the abscission of the terminal meristem at the end of the growth season, so Distribution that elongation of branches happens through The family is pantropical (Fig. 1, 4, 5, 6, 7 & 8). the meristem of the upper lateral bud. The The majority of the genera are truly tropical, buds are scaled. Even truly tropical lowland but Ficus extends with some species to the sub­ species of these genera, Brousonettia greveana

Fig. 7. Distribution of two tribes of Moraceae [Moreae and Castilleae] with the numbers of species for each. Continuous lines for primary centres, broken lines for secondary ones. Thick broken lines for strong links between partial areas. Con­ tinuous and broken lines and arrows for main distribution tracks. Small circle for Moreae in Africa for Militia. 438 BS 55

Fig. 8. Outline of the distribution of the Ficeae. Major concentrations on species indicated by triangles, lesser concentra­ tions by circles.

(Baill.) C.C. Berg (Madagascar) and Morus family in the main phytogeographic becomes mesozygia A. Chev. (Africa), show these features more balanced, with regard to the numbers of (Berg 1977b). both species and genera. Most tropical Moraceae grow in humid low­ Based on distribution patterns of tribes and land forest, relatively few are montane or sub­ of sections or subsections of Ficus, primary and montane species or are found in drier condi­ secondary centres can be recognized. tions such as seasonal forests, or even in semi­ In the Neotropics, the northern Andes desserts. region and the adjacent part of Central Ameri­ The tribes Castilleae (Fig. 7) and Dorste- can and the (upper) Amazon basin are pri­ nieae (Fig. 6) show a clear trans-Atlantic (West- mary centres and the Guianas, eastern Brazil, Gondwanan) connection. The other tribes do and southern Mexico and the adjacent part of not. The Soroceae is the only tribe confined to Central America (with an extension to Greater the Neotropics, and the tribe “Antiaropsideae” Antilles) are secondary centres. (ined.) is confined to New Caledonia and New The primary centres in Africa are (humid Guinea. The Artocarpeae and Moreae are cen­ western) Central Africa and (± dry) eastern tred in Malesia and the Sino-Himalayan region and northern Africa (with an extension to Ara­ respectively; both are represented by a single bia); secondary centres are (humid) western genus in Africa. The Ficeae are centred in Africa, (± humid) eastern Africa, and Madagas­ southeast Asia (Fig. 4, 5 & 8); some subgenera car. have (secondary?) centres in the Neotropics, Three main centres can be recognized in Africa, and/or Australia. It is not possible to Asia: the Sino-Himalayan region, western Male­ indicate a hypothetic centre of origin for the sia (with northern Borneo as a hotspot), and whole family. The richness of species in SE Asia eastern Malesia (with eastern New Guinea as a is largely caused by “explosive” speciation in hotspot). The only rather clear secondary cen­ (gyno)dioecious segment of the genus Ficus', tre is Peninsular (and Sri Tanka). disregarding this fact, the representation of the Other centres are northern Australia for BS 55 439

Ficus subsect. Malvanthera (of sect. Stilpnophyl- cation of African Moraceae compared with those of lum) the Pacific (with New Caledonia as other tropical areas. In: Huxley, C.R., Lock, J.M. & Cut­ hotspot) for Ficus sect. Oreosycea subsect. Glan­ ler, D.F. (eds.), Chorology, Taxonomy and Ecology of the Flo­ ras of Africa and Madagascar. Royal Botanic Gardens, Kew. dulosae (E austrocaledonica-growp), see Fig. 4 Pp. 131-148. and 8. Berg, C.C. 2001. Moreae, Artocarpeae, Dorstenia The number of genera represented in the (Moraceae). With introductions to the family and Ficus main phytogeographical regions is rather simi­ and with additions and corrections to Flora Neotropica lar, but the number of endemic genera differs Monograph 7. Fl. Neotrop. Monogr. 83: 1- 346. Berg, C.C. 2003. Flora Malesiana precursor for the treat­ clearly, and so does the number of species (Fig. ment of Moraceae 1 : the main subdivisions of Ficus: the 1). The high number of species in the Asian- subgenera. Blumea 48: 168-178. Australasian region is caused by explosive radi­ Berg, C.C. & Hijman, M.E.E. 1999. The genus Dorstenia ation of the the (gyno) dioecious groups of (Moraceae). Ilicifolia 2: 1-211. Ficus. Berg, C.C. & Wiebes, J.T. 1992. African figtrees and fig wasps. Verhandelingen der Koninklijke Nederlandse Akademie van Wetenschappen, Afd. Natuurkunde, 89. Corner, E.J.H. 1958. An introduction to the distribution of Literature cited Ficus. Reinwardtia 4: 15-45. Corner, E.J.H. 1960. Taxonomic notes on Ficus Linn., Asia Baas, P., Wheeler, E. & Chase, M. 2000. Dicotyledonous and Australasia, I-VI. Gard. Bull. Singapore 17: 368-404, wood anatomy and the APG system of angiosperm classi­ 405-415, 416-441, 442-485; 18: 1-35, 36-69. fication. Bot. J. Linn. Soc. 134: 3-17. Corner, E.J.H. 1962. The classification of Moraceae. Gard. Bâillon, H.E, 1875. Ulmacées. In: Histoire des plantes. Vol. 6. Bull. Singapore 19: 187-252. L. Hachette & Cie, Paris, London, Leipzig. Pp. 137-216. Corner, E.J.H. 1965. Check-list of Ficus in Asia and Aus­ Balslev, H. & Renner, S.S. 1989. Diversity of Ecuadorian tralasia with keys to identification. Gard. Bull. Singapore forests. In: Holm-Nielsen, L.B., Nielsen, EC. & Balslev, H. 21: 1-186. (eds.), Tropical Forests — Biological Dynamics, Speciation and Cronquist, A. 1981. An Integrated System of Glassification of Diversity. Academic Press, London & San Diego. Pp. 287- Flowering Plants. Columbia University Press, New York. 295. Eichler, A.W. 1875. Blüthendiagramme. Leipzig: Engelmann. Bentham, G. 1880. Urticaceae. In: Bentham, G. & Hooker, Engler, G.H.A. 1889. Moraceae. In: Engler, G.H.A. & J.D. (eds.), Genera plantarum. Vol. 3(1). L. Reeve Co., Prantl, K. (eds.), Natürlichen Pflanzenfamilien. Vol. 3(1). London. Pp. 341-395. Wilhelm Engelmann, Leipzig. Pp. 66-98. Berg, C.C. 1972. Olmedieae, Brosimeae (Moraceae). Fl. Gasparrini, G. 1844. Nova genera, quae supper nonnullis Fid Neotrop. Monogr. 7: 1-229. specibus struebat. Napoli. Berg, C.C. 1977a. Urticales, their differentiation and sys­ Gasparrini, G. 1845. Ricerche sulla natura del Caprifio, e del tematic position. Pl. Syst. Evol. (Suppl.) 1: 349-374. Ficus e sulla caprificazione. Napoli. Berg, C.C. 1977b. Revisions of African Moraceae (exclud­ Gentry, A.H. 1993. Diversity and floristic composition of ing Dorstenia, Ficus, Musanga and Myrianthus). Bull. lowland tropical forest in Africa and South America. In: Jard. Bot. État 47: 267-407. Goldblatt, P. (ed.), Biological Relationships between Africa Berg, C.C. 1983. Dispersal and distribution in Urticales - and South America. Yale University Press, New Haven & an outline. Sonderb. Naturwiss. Vereins Hamburg 7: 219- London. Pp. 500-547. 229. Jarrett, F.M. 1959-1960. Studies in Artocarpus and allied Berg, C.C. 1989. Systematics and phylogeny of the genera, I-V. J. Arnold Arbor. 40: 1-37, 113-155, 298- 368; Urticales. In: Crane, P.R. & Blackmore, S. (eds.), Evolu­ 41: 111-140, 320-340. tion, Systematics, and Fossil History of the Hamamelidae. Vol. Koek-Noorman, J., Topper, S.M. & ter Welle, B.J.H. 1984. 2. Higher' Hamamelidae. Systematics Association, Spec. The systematic wood anatomy of the Moraceae. III. Vol. 40B. Clarendon Press, Oxford. Pp. 193-220. Tribe Ficeae. I.A.W.A. Bull., N.S. 5: 330-334. Berg, C.C. 1990. Differentiation of flowers and inflores­ Miquel, F.A.G. 1847-1848. Prodromus Monographiae cences of Urticales in relation to their protection against Ficuum. London J. Bot. 6: 514-588; 7: 64-78, 109-116, 221- breeding insects and to pollination. Sommerfeltia 11: 13- 236, 425-471. 34. Miquel, F.A.G. 1867. Annotationes de Ficus speciebus. Berg, C.C. 1998. Phytogeography, systematics and diversifi­ Ann. Mus. Bot. Lugduno-Batavum 3: 260-315. 440 BS 55

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