Ficus

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Ficus

Description

Trees, shrubs or climbers, often with adventitious roots (aerial in hemi-epiphytes and root-climbers), monoecious or (gyno)dioecious (functionally ‘male’ and ‘female’); — The genus shows a wide range of life- and growth-forms.
— The leaves are spirally arranged (as nearly always in subg. Pharmacosycea and subg. Urostigma, the exceptions being some African species of the latter subgenus with subopposite leaves, as well as in subg. Ficus). The leaves are predominantly distichous in subg. Synoecia, but may in some species vary to the arrangement in lax spirals. In the other two subgenera, Sycidium and Sycomorus, the leaves are arranged spirally or distichous, but in the former subgenus the leaves are sometimes subopposite.
Leaves spirally arranged, distichous, (sub)opposite or sometimes subverticillate; stipules fully amplexicaul to lateral, mostly free. — The stipules are fully amplexicaul in the majority of the Ficus species, giving annular scars. In many species, possibly all species of dioecious groups, the stipules are not fully amplexicaul in juvenile stages. The stipules are, however, fully amplexicaul, giving annular scars, in the majority of the species in the adult state. The juvenile trait is retained in many species of subg. Sycidium, having semi-amplexicaul to lateral (subulate) stipules. In some species (as F. ampelas) both fully amplexicaul and not fully amplexicaul stipules can be found, even on the same twig. Not fully amplexicaul stipules also occur in subg. Ficus subsect. Frutescentiae. These are correlated with Terminalia-growth. Semi-amplexicaul to lateral stipules are found on the lower nodes of the branches, upwards they are usually fully amplexicaul, but not so in F. ischnopoda and F. tuphapensis (from China and Indochina). The stipules may be persistent or subpersistent along the leafy twigs and may hide the figs. In several groups with intermittent growth the distal internodes of the twigs can be very short and the stipules persistent, in small apical tufts as in subg. Ficus subsect. Frutescentiae and subg. Sycidium sect. Sycidium, or scale-like and forming terminal buds as in subg. Urostigma subsect. Urostigma.

The stipules are often conspicuous as terminal bud covers. They can be longer than 10 cm in F. elastica and F. insipida Willd. (Neotropics). Stipules on opening shoots (flush) can be much longer than those of normally growing branches.

In numerous species of subg. Urostigma, the figs are initially enclosed in calyptrate bud covers, usually with texture and indumentum similar to those of the stipules. They are formed by two fused scale-leaves (or prophylls) subtending the inflorescences (Golenkin 1894; Bernbeck 1932). These bud covers are mostly small, but in some specious conspicuous, even up to 2.5 cm long in F. cucurbitina. The calyptrate bud cover pairs may enclose single figs as is often the case in subsect. Conosycea or pairs as in some species of this subsection, e.g., F. glaberrima. Enclosure of pairs of figs is usual in sect. Galoglychia (Africa) and sect. Americana. In the latter case the scale-leaves are apparently the prophylls.
The inflorescences of Ficus, the syconia or figs, are unique as they enclose both staminate and pistillate flowers during anthesis. Urceolate inflorescences are also found in Sparattosyce, but in this genus the stigmata are outside the opening of the receptacle and the staminate inflorescences split open to expose the anthers. One can consider the basic structure to be an involucrate discoid head, similar to that of Compositae, except for the cymose arrangement off the flowers (; Corner 1978). This could be so for subg. Sycidium and for subg. Sycomorus (at least pro parte), or even for subg. Pharmacosycea in which both in the Old and New World lateral bracts occasionally occur, but for those subgenera not showing any trace of lateral bracts, Ficus, Synoecia, and Urostigma, it is doubtful. The occurrence of caducous basal bracts in the latter two subgenera makes it uncertain whether basal bracts and ostiolar bracts (which are always persistent) are (fully) homologous. The constant numbers of basal bracts (and even peduncular bracts) may also indicate lack of full homology.

The enclosure of the flowers is realized by the involution of the margins, leaving only a narrow entrance, the ostiole. In several species of subg. Sycidium and subg. Sycomorus all the bracts persist, but in the majority most of the bracts disappear. In all subgenera the margin of the receptacle bears many rows of imbricate and often interlocking bracts, as ostiolar bracts closing more or less tightly the entrance to the interior of the fig. In most subgenera a whorl of 2 or 3 bracts remained at the base of the receptacle, basal bracts. In most species of subg. Sycidium and in some species of subg. Pharmacosycea, the 2 or 3 bracts occur not in a whorl but scattered on the peduncle, peduncular bracts. The bracts on the outer surface of the receptacle, lateral bracts, are found in many species of subg. Sycidium and subg. Sycomorus; they are occasionally found in subg. Pharmacosycea, but are absent in the other subgenera. Lateral bracts can be large and numerous, (largely covering the outer surface of the receptacle) or few and then mostly small and scattered. Bracts (often in constant numbers) surrounding the ostiole are indicated as apical bracts. Bracts among the flowers, interfloral bracts, occur only in the subgenera Pharmacosycea and Urostigma; in subg. Pharmacosycea, the interfloral bracts are often on the pedicel, sometimes up to the perianth and indistinguishable from the tepals. Interfloral bracts are absent in the other subgenera; in subg. Sycomorus, however, two (or three) bracteoles subtend the staminate flowers in the majority of the species (see, e.g., ; ; ; ). The inner surface of the receptacle can be hairy, mostly with bristle-like hairs. Such hairs are common in the groups with dioecious species (subgenera Ficus, Sycidium, Sycomorus for the greater part, and Synoecia), but are also found in some groups of subg. Urostigma (subsect. Urostigma) and subg. Pharmacosycea (subsect. Pedunculatae).

The syconia are sessile or pedunculate. In numerous species, both with pedunculate and sessile figs, the base of the receptacle is stipitate. Stipes are rare in subg. Urostigma and occur in general in Malesia more frequently than in Africa (found in F. cyathistipula and some related species of sect. Galoglychia) and the Neotropics (found in some species of sect. Pharmacosycea: F. guajavoides Lundell and F. tonduzii Standl.). The shape of the receptacle is (almost) globose, but varies to depressed-globose to pyriform to ellipsoid to oblongoid or to cylindrical. The receptacle varies in size from 2-3 mm in diameter when dry (as in several species of subg. Sycidium sect. Palaeomorphe) to about 10-13 cm in F. dammaropsis. Figs of such dimensions are uncommon, they can be found in some species of subg. Synoecia (e.g. F. punctata) and of subg. Sycomorus (e.g. F. auriculata); the up to 10 cm long ellipsoid figs of F. hesperidiiformis (of subsect. Malvanthera) may also be included in this category. Such large figs are even rarer in other parts of the tropics; they are known from a Madagascan form of F. sycomorus L. (‘F. skalavarum’), from the African F. sansibarica Warb., and the neotropical F. gigan- tosyce Dugand. The often considerable variation in size of the receptacle (and, consequentially, also the number of flowers per inflorescence) in many species is a remarkable phenomenon.

The receptacle remains closed in nearly all species. In some species of subg. Ficus subsect. Eriosycea, ‘gall-figs’ split open at maturity; this is also found in the African F. asperifolia (subg. Sycidium).

The receptacles of many species of subg. Sycomorus are filled with watery to gelatinous liquid during the interfloral phase. Such liquid rarely occurs in species of other groups; its presence is known for F. conocephalifolia (of subg. Sycidium); it is also found in some species of subg. Urostigma sect. Galoglychia (subsect. Caulocarpae) and sect. Americana (pers. comm. F. Kjellberg). Males of fig wasps, both pollinating ones and others, are provided with respiratory adaptations to this environment; leaving the ‘gall-fruits’ before the females, they may still encounter liquid in the fig (Compton & McLaren 1989).
Inflorescences with an urceolate receptacle (syconium or fig) with a narrow circular or slit-shaped orifice (ostiole), bracts on the peduncle (peduncular bracts), subtending the receptacle (basal bracts, mostly 2 or 3); on the outer surface of the receptacle (lateral bracts), in the orifice of the receptacle (ostiolar bracts), among the flowers (interfloral bracts) and/or subtending (staminate) flowers (bracteoles). — The flowers are unisexual, at least functionally. The perianth is and remains both in staminate and pistillate flowers membranaceous. The number of tepals vary from (2 or) 3 to 6. They are free or connate, and glabrous or hairy. Their colour varies from whitish to red.
Fruit a drupelet or achene, small. — The pericarp consists of (two) or three layers of cells. The cells of the inner layer (endocarp) becomes sclerified and is the protective layer around the seed (Johri & Konar 1956; Verkerke 1986). In many species the whole pericarp becomes dry and achene-like; however, in others the fruit is subdrupaceous with a thin fleshy layer or drupaceous with a thick fleshy layer. In the subdrupaceous fruit the other layer form mucilage in water which makes the layer viscid so that the fruit can be glued to surfaces of animals, etc. (Ramirez 1976). The layer is not or hardly affected by passage of the fruit through the digestive track of frugivores and it contains lipids, e.g. in F. microcarpa (Kaufmann et al. 1991). The contents make the layer attractive to ants (see p. 61) and appears to inhibit germination (see p. 61). In some groups the fruits are more or less clearly drupaceous. In the F. montana-group (subg. Sycidium sect. Sycidium) and the related African species there are dehiscent drupelets with a white exocarp, squeezing out (or expulsing?) the endocarp body, which is almost tetrahedral in shape and has a tuberculate surface (). In some subsections of Galoglychia, the African section of subg. Urostigma also have dehiscent drupelets or fruits with a partly fleshy or mucilaginous outer layer showing clear morphological similarities to the characteristic Moraceous dehiscent drupe (Berg & Wiebes 1992: 29). The fleshy layer of the pericarp is whitish. One need to have fresh material to analyse the structure of the pericarp, in particular the presence of fleshy layers. The fruitlets as a whole are in herbarium material entirely or partly red to red-brown or whitish, differences that can play a role in distinguishing species. The pericarps of ‘gall-fruits’, in which the fig insects develop, become entirely dry and have a smooth surface. They are usually thinner than those of true fruits, so that (dark-coloured) insects are visible (see Verkerke 1986). Moreover, the shape of the ‘gall-fruit’ tend to be different, often obovoid rather than ovoid. In addition to true fruits and ‘gall-fruits’, one can find ‘bladders’, empty swollen ovaries in which wasps (or seeds) have not developed (Galil & Eisikowitch 1971) and/or abnormally developed ‘fruits’, often large and/or with unusual shapes, caused by gall-making insects (see Cook & Rasplus 2003). In the dioecious groups, the pericarps containing seeds vary in shape from compressed to subglobose, in outline from elliptic to subreniform to oblong. They are often keeled and/or tuberculate (). Certain features of the fruits are more or less characteristic for certain subdivisions, such as the ± compressed and in outline elliptic to oblong fruits with a keel all around () for subg. Synoecia, those with a basal double keel () for sect. Adenosperma (of subg. Sycomorus), and those with a prominent pseudohilum () for subsect. Sycocarpus (of subg. Sycomorus). The fruits of the monoecious subgenera Pharmacosycea and Urostigma are either lenticular or somewhat oblongoid and plump. They show little or no variation in most subdivisions. However, the African sect. Galoglychia (of subg. Urostigma) shows a considerable variation (Berg & Wiebes 1992).The fruits varies in size from 0.5 to 5 mm in length. The style is usually caducous, but it is persistent in the fruit of F. macrostyla and F. squamosa. These styles have an unusual length and bear stiff retrorse hairs. Both species are rheophytes and it is likely that the fruit and style construction promotes attachment of the fruits to the substrate. The fruits of subsect. Malvanthera (subg. Urostigma) are mostly partly or entirely embedded in the wall of the syconium (see above).
Seed with endosperm, embryo (almost) straight with flat and equal cotyledons or ± curved with conduplicate cotyledons. — The embryo is either straight with cotyledons which are equal and flat or ± curved with a relatively long radicle and conduplicate cotyledons of which the smaller is partly enveloped by the larger one (). The latter type is found in relatively large seeds (in relatively large fruits). The seeds contain endosperm, although in rather small amounts. Seeds can remain dormant for long periods, at least several years, in dry and cool (artificial) conditions.

Distribution

Africa: present America: present Asia-Tropical:, Borneopresent; Jawa (Jawapresent); Lesser Sunda Is.present; Malaya (Peninsular Malaysiapresent); Maluku (Malukupresent); New Guineapresent; Philippines (Philippinespresent); Sulawesi (Sulawesipresent); Sumatera (Sumaterapresent); Thailand (Thailandpresent) Asian-Australasian region: present Australasia: Eastern New Guinea: present Myanmar: present Pantropical: present Sino-Himalayan subregion: present between Java: present from S Japan to Taiwan and Cambodia: present northern Borneo: present
The genus is pantropical, extending to subtropical (or warm temperate) regions. It comprises c. 735 species, of which c. 120 in America, c. 105 in Africa (continent, Madagascar and other Indian Ocean islands, and the Arabian Peninsula), and the others in the Asian-Australasian region; 367, including five introduced ones, occur in Malesia; for the distribution in Malesia see Table 1.

America has two endemic sections, subg. Pharmacosycea sect. Pharmacosycea and subg. Urostigma sect. Americana, both with affinities to the Asian-Australasian sections of these subgenera, but not to the African Ficus flora. Subgenus Urostigma sect. Galoglychia is endemic to Africa (Madagascar, adjacent Indian Ocean islands, and the Arabian Peninsula). It is quite distinct from the Asian section, but shows affinities to sect. Stilpnophyllum, centred in Australia. Subgenus Sycomorus subsect. Sycomorus, is, in contrast to the majority of the subgenus, monoecious and subendemic to Africa (and Madagascar, adjacent Indian Ocean islands, and the Arabian Peninsula); Ficus racemosa is the only Asian species of this subsection and ranges from Sri Lanka and Pakistan to Australia. All other Ficus species of the African continent belong to groups centred in Asia, the species of more or less dry types of African vegetation are linked to groups represented in western Asia (subg. Urostigma subsect. Urostigma, subg. Pharmacosycea subsect. Pedunculatae, subg. Sycidium sect. Sycidium, and F. heterophylla/montana-groups). There are two species occurring both in Africa and Asia: F. exasperata Vahl and F. palmata Forssk.; F. carica extends to the Mediterranean. Like in other genera, the Madagascan species not belonging to (sub)endemic African groups tend to show affinities to Malesian groups.

Three centres are found in the periphery of the extensive Asian-Australasian region: New Caledonia with the F. austrocaledonica-group of subg. Pharmacosycea, Australia with subsect. Malvanthera of subg. Urostigma, the Sino-Himalayan subregion with subsect. Frutescentiae of subg. Ficus and subsect. Plagiostigma (and subsect. Pogonotrophe) of subg. Synoecia. Two major groups of species can be recognized in Malesia: a western Malesian group, dominated by species of the subgenera Ficus, Synoecia, and Urostigma, and with a clear centre in northern Borneo, and an eastern Malesian group, dominated by the subgenera Pharmacosycea, Sycidium, and Sycomorus, with a clear centre in eastern New Guinea. The two groups meet in the Philippines. The Sino-Himalayan region harbours some odd species or groups of species: F. elastica is clearly related to the Australian species of subsect. Malvanthera, F. auriculata and the closely related F. hainanensis Merr. & Chun are both related to the New Guinean species of subsect. Neomorphe. Ficus henryi Diels is probably related to the mainly New Guinean F. conocephalifolia-group of subg. Sycidium, and furthermore F. griffithii (Miq.) Miq. (subsect. Sycocarpus), F. semicordata and two allied species constituting sect. Hemicardia (subg. Sycomorus), and F. laevis of the monotypic subsect. Pogonotrophe (subg. Synoecia) without close relatives.

All groups comprise one or some species with very wide distribution, e.g. subg. Ficus with F. hirta and F. lamponga, subg. Pharmacosycea with F. albipila and F. nervosa, subg. Sycidium with F. subulata and F. tinctoria, subg. Sycomorus with F. racemosa and F. variegata, subg. Synoecia with F. disticha and F. punctata, and subg. Urostigma with F. microcarpa and F. virens.

Most species have more or less coherent ranges of distribution, a few are evidently disjunct in their distribution: F. anastomosans occurring on limestone in Thailand and Myanmar and in Celebes; F. opposita in New Guinea and Australia and in an islet in the Sunda Strait (between Java and Sumatra); and F. subpisocarpa ranging from S Japan to Taiwan and Cambodia and in Ceram (Moluccas). The general patterns of distribution and of diversification strongly suggest that the genus originated in eastern Gondwana with currently the two main centres in western Malesia (with northern Borneo as a hotspot) and the Sino-Himalayan region linked to it and eastern Malesia (with New Guinea as a hotspot) and the Pacific region linked to it. More or less isolated from centres are the Africa ‘block’ with the morphologically more or less distinct subdivisions sect. Galoglychia and subsect. Sycomorus, and the Australian ‘block’ with subsect. Malvanthera. The occurrence of two sections in the Neotropics is the more peculiar as they show clear morphological relations to Asian-Australasian groups.
SumatraMalay PeninsulaJavaBorneoLesser Sunda IslandsMoluccasTable 1. Indigenous or naturalized (*F. hirta) Malesian species. Uro = subg. Urostigma; Pha = subg. Pharmacosycea; Fic = subg. Ficus; Soe = subg. Synoecia; Syc = subg. Sycidium; Syo = subg. Sycomorus; = uncertain number.
UroPhaFicSoeSycSyoTotal
Sumatra32 (33)513141614 (15)94 (97)
Malay Peninsula4341315101499
Java2857*11158 (9)74 (75)
Borneo38 (40)42025 (26)2625138 (141)
Philippines255813201687
Celebes18 (20)7962216 (17)78 (81)
Lesser Sunda Islands124138634
Moluccas14 (15)457 (8)162379 (81)
New Guinea18142242951139

Ecology

The species of Ficus are mainly tropical. Comparatively few are subtropical and but two can be regarded as subtemperate, namely F. carica of southern Europe and Asia Minor, and F. sarmentosa Buch.-Ham. ex Sm. of Japan, Korea, and China. These two species may reach the latitude of 40° N in Europe and Japan but in general the limits of the genus lie between the latitudes of 35° N and S. In Asia F. heteromorpha Hemsl. occurs to c. 35° N as in China (Shensi and Honan) and in southern Korea F. erecta. In Australia F. coronata Colla occurs in Mallacoota in Victoria (37° 30' S). In Africa the genus ranges from Egypt (F. sycomorus L.) and Algeria (F. cordata Thunb. subsp. salicifolia (Vahl) C.C. Berg) to the Cape of Good Hope (F. sur Forssk.). In America from southern Florida (F. aurea Nutt. and F. citrifolia Mill.) and north-western Mexico (F. petiolaris Kunth) to Uruguay and northern Argentina (F. luschnathiana (Miq.) Miq.).

The megatherm nature of the genus is also reflected in its altitudinal distribution. Most of the tropical species occur in lowland and submontane zones below 1500 m. A small number occur in the montane zone between 1500 and 2400 m, but above this there are few records. Thus some Andean species have been collected at 3000 m (F. andicola Standl.) or even at 3200 m (F. cuatrecasana Dugand). Ficus oleifolia has been found at 3200 m on Mt Kinabalu (Borneo). In New Guinea, F. endochaete, F. quercetorum, and F. saccata are montane species, typical of the Nothofagus forests up to 2400 m. Most species belong to vegetation subject to an ever-wet climate, but there are several which seem to be indifferent to the distribution of rainfall and can extend into the typical monsoon climate. Here they are not necessarily restricted to riversides and wells (the sumbers of East Java), but they are found also in places where soil dries out, such as teak forests. Among these are F. albipila, F. punctata, and F. subcordata, all of which thrive also in rainforest. A few species, however, seem characteristic of drier climates, such as F. brachypoda and F. opposita.

The role of Ficus in Malesian vegetation is important because almost every vegetation or biotype below the subalpine zone has one or more common species, important both to construction of vegetation and to food-supply of animals.

The genus is absent in mangroves, but some species, as F. microcarpa, can often be found in brackish swamp. Many species occur in fresh water swamps, in western Malesia, e.g. F. callophylla, F. consociata, F. crassiramea, and F. sundaica. In western Malesia, large terrestrial trees with the capacity to produce tall trunks are not common. Those found in this region are F. variegata of subg. Sycomorus and some species of subg. Pharmacosycea, F. magnoliifolia and F. nervosa. However, in New Guinea such trees, often buttressed and more than 30 m tall, make up a considerable proportion of the forest. They are species of subg. Pharmacosycea, subg. Sycidium, and subg. Sycomorus (sect. Adenosperma and subsect. Neomorphe). The smaller trees of these subgenera and subg. Ficus are mostly species of riversides and belong to the understories of the forest. Others are more characteristic of open places, particularly landslips, whence they come to abound in secondary vegetation at altitudes up to 1500 m. This secondary vegetation in Borneo, is characterized by a great abundance of flagelliflorous (geocarpic) species of sect. Sycocarpus (subg. Sycomorus), and of species of subsect. Auratae (subg. Ficus). Several secondary growth species, in particular those of subsect. Eriosycea (subg. Ficus), such as F. fulva, F. grossularioides, F. hirta, and F. padana, may behave as weed-trees and may form almost pure stands.

Hemi-epiphytic species often invade villages, orchards, and town-gardens, establishing themselves on trees and walls (Fig. 1). They can also often be found on limestone hills, rocky cliffs, and rocky headlands by the sea.

The root-climbers of subg. Synoecia, seem mostly to require a shade-phase to establish themselves. They do not participate in the initial tangle of climbers which so often develop in early stages of secondary forest.

Several species are rheophytic and can thus be found in and along swift rocky streams (see p. 27). Ficus is scarce on very sterile soil, such as the leached sands of padang and kerangas, probably because of the need of an ample nutrient supply to ensure by flower-production the maintenance of the pollination system. Species adapted to nutrient-poor conditions are F. deltoidea and F. oleifolia, which both can be holo-epiphytic and are distinct by the phenology of the fig production. Ficus can play an important role in colonisation of volcano islands, as demonstrated for the Krakatau Islands between Java and Sumatra and Long Island near Papua New Guinea (Thornton et al. 1996; Shanahan et al. 2001).
X. Shanahan, M., R.D. Harrison, R. Yamuna, W. Boen & I.W.B. Thornton, Colonization of an island volcano, Long Island, Papua New Guinea, and an emergent island, Momot, in its caldera lake V. Colonization by figs (Ficus spp.), their dispersers and pollinators. in J. Biogeogr. 28. 2001, Y. Thornton, I.W.B., S.G. Compton & C.N. Wilson, The role of animals in the colonization of Krakatau Islands by fig trees (Ficus species) in J. Biogeogr. 23. 1996

Dispersal

The majority of the Ficus species are dispersed by animals. The ripe figs are mostly eaten at the spot; small figs are swallowed and the fruits (or pyrenes) pass the digestive tracts and are released in the droppings. Monkeys and squirrels have the tendency to eat a bit of a fig and drop most of it. Squirrels and fruit bats may carry figs to other places to eat them there. Endo-zoochory and dys-zoochory (the diaspores are eaten and digested) are the most common mode of the dispersal of seeds of Ficus. Exo-zoochorous dispersal happens when only the fruitlets are eaten from the syconia, as by pigeons. The fruitlets may stick to the bill and be brushed off to branches. Water plays a role in dispersal by transporting floating figs. The African F. cyathistipula is adapted to this mode of transport by a thick spongy wall of the syconium. For F. macrostyla and F. squamosa the single fruitlets are probably essential entities of dispersal. In these rheophytic species the very long styles are persistent. These styles have short and stiff retrorse hairs which will contribute to attachment to the substrate.

The colour of ripe figs vary from green to yellow to orange to red to purple or blackish. A more extensive and detailed overview was presented by Shanahan et al. (2001) in a global review of fig-eating vertebrate frugivores. It treats the groups of animals involved (birds, arboreal and terrestrial mammals, reptiles and fishes), their effectiveness as seed-dispersers, syndromes mainly based on dimension and colour of the syconia and their position on the tree (or height in the vegetation) and groups of animals associated with them, and figs as keystone resources (see also Lambert & Marshall 1991; Kinnaird et al. 1999). However, the importance of Ficus is not everywhere in the humid tropics the same (see Gautier-Hion & Michaloud 1989). Six dispersal guilds mainly determined by vertical stratification were recognized in Ficus in lowland rain forest in northern Borneo by Shanahan & Compton (2001).

Ants play a role in further dispersal of fruits deposited, e.g. on branches, as in droppings of animals. In this two-phase dispersal mechanism the ants are attracted by the lipid containing viscid outer layer of fruits and may carry the fruits to sites more suitable for germination and establishment (Kaufmann et al. 1991). On the other hand, ants harvesting fig fruits in the forest canopy and eating them, have negative effects upon frequency of establishment (Laman 1994). The traits of the fruits and seeds of Ficus allow long-distance dispersal. Events of long-distance dispersal will probably rarely result in reproduction and establishment by absence of pollinators and populations of trees to allow establishment of the pollinators as well.
CK. Bessey, E.A. - The Florida strangling figs in Ann. Rep. Missouri Bot. Gard. 1908, CL. Galil, J. & L. Meiri, Drupelet germination in Ficus religiosa L in Israel J. Bot. 30. 1981, CM. Gautier-Hion, A. & G. Michaloud, Figs: are they keystone resources for frugivorous vertebrates throughout the tropics? A test in Gabon in Ecology 70. 1989, CN. Johri, B.M. & R.N. Konar, The floral morphology and embryology of Ficus religiosa Linn in Phytomorphology 6. 1956, CO. Kaufmann, S., D.B. McKey, M. Hossaert-McKey & C.C. Horvitz, Adaptations for a two-phase seed dispersal system involving vertebrates and ants in a hemiepiphytic fig (Ficus microcarpa: Moraceae) in Amer. J. Bot. 78. 1991, CP. Kinnaird, M.F., T.G. O’Brien & S. Suryadi, The importance of figs to Sulawesi’s imperiled wildlife in Trop. Biodiversity 6. 1999, CQ. Laman, T.G. - in The ecology of strangler figs (hemi-epiphytic Ficus spp.) in the rain forest canopy of Borneo. 1994, CR. Lambert, F.R. & A.G. Marshall, Key stone characters of bird-dispersed Ficus in a Malaysian lowland rain forest in J. Ecol. 79. 1991, CS. Michaloud, G. & S. Michaloud-Pelletier, Ficus hemi-epiphytes (Moraceae) et arbres supports in Biotropica 19. 1987, CT. Midya, S. & R.L. Brahmachary, The effect of birds upon germination of banyan (Ficus benghalensis) seeds in J. Trop. Ecol. 7. 1991, CU. Ramirez B., W., Germination of seeds of New World Urostigma and of Morus rubra L in (Moraceae). Rev. Biol. Trop. 24. 1976, CV. Shanahan, M. & S.G. Compton, Vertical stratification of figs and fig-eaters in a Bornean lowland rain forest: how is the canopy different? in Plant Ecol. 153. 2001, CW. Shanahan, M., S. So, S.G. Compton & R. Corlett, Fig-eating by vertebrate frugivores: a global review in Biol. Rev. 76. 2001, CX. Verkerke, W., Sycone morphology and its influence on the flower structure of Ficus sur (Moraceae) in Proc. Kon. Ned. Akad. Wetensch. 91. 1988

Morphology

The genus is so diverse in many respects that it is comparable with a large family.

Major differentiating characters (the morphological characters that distinguish Ficus from (most) other genera of Moraceae) are:
  1. The flowers remain entirely enclosed in an urceolate receptacle (syconium) also during anthesis.
  2. Heterostyly (imperfect or perfect): the stigmas lined up (in monoecious taxa due to differences in length of the pedicel (or also shape of the ovary)).
  3. Pedicels of pistillate flowers are distinctly different in length in the same inflorescence.
  4. The number of staminate flowers (per inflorescence or per plant) is small in relation to the number of pistillate flowers.
  5. Membranous tepals of the pistillate flowers (also present in Broussonetia).
  6. Formation of a continuous, often coherent layer of stigmata (synstigma).
  7. Waxy glandular spots on the lamina beneath and/or on the nodes of leafy twigs.


Other differentiating characters:
  1. Pronounced protogyny: the staminate flowers are at anthesis when in the same inflorescence the seeds are (nearly) ripe.
  2. The perianth (and interfloral bracts + internal bristles) remains intact in spite of loss of their protective function.


Several of the generic features of the flowers and inflorescences are essential for the pollination system. They may be regarded as pre-adaptations to protection against damage by insect larvae rather than as adaptations to pollination. Also the watery to gelatinous liquid in the syconia (figs) of many species of subg. Sycomorus probably has (had) a protective function, and possibly even delayed male anthesis. Anthesis of pistillate flowers ahead of staminate ones in a bisexual inflorescence is not unusual in Moraceae, as in simple cymose inflorescences the pistillate flowers are formed on the proximal axes and the staminate ones on distal axes. The interval between female and male anthesis is normally some days and the interval of some weeks in Ficus is peculiar. Coincidence of anthesis of staminate and pistillate flowers in a not (yet) fully closed receptacle would have given opportunities to penetrate among flowers.
CY. Berg, C.C., A new species of Ficus (Moraceae) of uncertain origin in Brittonia 56. 2004, CZ. Bernbeck, F., Vergleichende Morphologie der Urticaceen- und Moraceen-Infloreszenzen in Bot. Abh. 19. 1932, DA. Beyrich, H., Über die Membranverkieselung einiger Pflanzenhaare in Flora 36. 1942, DB. Corner, E.J.H. in Wayside trees of Malaya 1. 1940, DC. Daniels, J.D. & R.O. Lawton, A natural history of strangling by Ficus crassiuscula in Costa Rican lower montane forest in Selbyana 14. 1993, DD. Daniels, J.D. & R.O. Lawton, Habitat and host preferences of Ficus crassiuscula, a neotropical strangling fig of the lower-montane forest in J. Ecol. 79. 1991, DE. Fedorov, A.A., Woody epiphytes and strangling figs in tropical forests of China in Bot. Zhurn (Moscow & Leningrad) 44. 1959, DF. Golenkin, M., Beiträge zur Entwickelungsgeschichte der Inflorescenzen der Urticaceen und Moraceen in Flora 78. 1894, DG. Harrison, R.D., A.A. Hamid, T. Kenta, H. Lafrankie, H.-S. Lee, H. Nagamasu, T. Nakashuzuka & P. Palmiotto, The diversity of hemi-epiphytic figs (Ficus: Moraceae) in a Bornean lowland rain forest in Biol. J. Linn. Soc. 78. 2003, DH. La Rosa, A., Il periderma picciolare di alcune specie di Ficus in Boll. Reale Orto Bot. Giardino Colon. Palermo, Nueva Ser. 2. 1921, DI. Michaloud, G. & S. Michaloud-Pelletier, Ficus hemi-epiphytes (Moraceae) et arbres supports in Biotropica 19. 1987, DJ. Prósperi, J., Biologie du développement des hémi-épihytes ligneux. 1998, DK. Rao, A.N., Developmental anatomy of natural root grafts in Ficus globosa in Aust. J. Bot. 14. 1966, DL. Van Steenis, C.G.G.J. - in Rheophytes of the World. 1981

Taxonomy

— The only monograph of Ficus is Miquel’s (1867). It is based on his Prodromus (1847-1848), where he distinguished several genera on floral details, as Gasparrini had just indicated (1844, 1845). As species were added, the distinctions diminished and the practical difficulty arose when sterile material, needing identification, could not be assigned to the genera. In 1867, therefore, Miquel submerged them into one genus, as subgenera or sections to accommodate 472 species recognized; this treatment has persisted. In his revision of the Asian and Malesian species, King (1887-1888) introduced two new sections (Palaeomorphe and Neomorphe), but retained most of Miquel’s subgenera and sections. He was concerned chiefly with the reduction of species and he limited his appreciation of the unsatisfactory state of the sectional classification by citing numerous exceptions.

Mildbraed & Burret (1911) were concerned with African species, most of which belong to one group, called by them subg. Bibracteatae (= subg. Urostigma sect. Galoglychia). The value of this taxon could not be estimated while the Asian and Australasian complement was still lumped into another group of Urostigma.

Elmer (1937) planned a superficial treatment of the Philippine species which was partly taken up and validated by Sata (1944). Sata introduced many new infrageneric names, but his standpoint was, indeed, too insular, and many antedating names coined by Endlicher (1850) and Miquel were overlooked.

Diels (1935) endeavoured to accommodate the New Guinea species into King’s classification, but he failed largely to follow Miquel’s advice on floral construction and he missed the keys to the revision of the genus which rich discoveries from Borneo to the Solomon Islands, New Caledonia, and Queensland necessitated.

Miquel’s advice on floral construction was followed by Corner, who undertook the tremendous task to revise the genus for an extensive area with a proliferation of names and many new discoveries. He did not only pay careful attention to floral construction, but also to characters of the fruit or pyrene (by Corner consequently indicated as seed) and anatomical details, as pioneered by Renner (1907). This resulted in a classification with nearly 125 infrageneric entities, subgenera to subseries, for the Asian-Australasian region (Corner 1965: 3-6). The subdivision was into a group of monoecious species, comprising three subgenera, Pharmacosycea (with 2 sections world-wide: Oreo- sycea and Pharmacosycea), Sycomorus, and Urostigma (with 7 sections world-wide; Americana, Conosycea, Galoglychia, Leucogyne, Malvanthera, Stilpnophyllum, and Urostigma), and a group of dioecious species, all Palaeotropical and accommodated in subg. Ficus, which was subdivided into 8 sections: Adenosperma, Ficus, Kalosyce, Neomorphe, Rhizocladus, Sinosycidium, Sycidium, and Sycocarpus.

Berg (1986) proposed the subdivision of the African section Galoglychia into 6 subsections and Carvajal & K.-Shabes (1998) of the American section Pharmacosycea into 2 subsections. A revision of the subdivision of the sect. Americana proposed by Miquel (1867) is in preparation (Berg in Berg & Villavicencio 2004).

The focus in Corner’s work on details distracted to some extent attention from macro-morphological characters of vegetative parts. This affected the construction of keys and the classification. That classification was questioned by Ramirez (1977) who suggested changes to get it more in accordance with pollinating fig wasp classification. Taxonomic studies on African Ficus species also raised questions and suggestions for changes in Corner’s classification (Berg 1989a, 1989b, 1998).

Revised classification — The current study on Malesian species created a possibility to check more closely upon Corner’s classification. This led to the currently proposed classification of the genus. It is primarily based on morphological criteria and takes into account various comments by Corner (1960, 1967) on the classification he proposed. He suggested to consider a separate subgenus combining the sections Kalosyce and Rhizocladus (1960) and to include the sections Adenosperma, Neomorphe, and Sycocarpus, but also the series Prostratae and Pungentes (of sect. Sycidium) in subgenus Sycomorus, if unifying characters could be found (1967).

The currently adopted classification, outlined by Berg (2003) comprises 6 subgenera: Two with only monoecious species: Pharmacosycea (with the sections Oreosycea and Pharmacosycea) and Urostigma (with the sections: Americana, Galoglychia, Stilpnophyllum, and Urostigma), Sycomorus (with dioecious and monoecious species and with the sections Adenosperma, Bosscheria, Dammaropsis, Hemicardia, Papuasyce, Sycocarpus, and Sycomorus), and three subgenera with only dioecious species: Ficus (with the sections: Eriosycea and Ficus), Sycidium (with the sections Palaeomorphe and Sycidium), and Synoecia (with the sections Kissosycea and Rhizocladus). Most of the sections comprise subsections, but the ranks of series and subseries are not applied, but instead informal groups of presumably related species indicated. The subgenera and most of the sections can be recognized on the basis of characters of vegetative parts and of the exterior of the fig. Three pairs of subgenera can be distinguished not only on the basis of morphological similarities but also of distribution patterns (Berg 2003): Pharmacosycea and Urostigma, Ficus and Synoecia, and Sycidium and Sycomorus.

This new classification also makes distribution patterns more transparent, and still support Corner’s grand visions regarding evolution and biology of the genus. The proposed classification is at least at level of subgenera, but also at the levels of sections and/or subsections largely in accordance with the taxonomy of the group of pollination fig wasps (Agaonidae). There are only few cases in which the wasp genus does not match the subgenus or section of Ficus. Moreover, analyses partly based on a molecular study by Weiblen (2000) largely supports this classification which is exclusively based on morphological criteria. A more recent molecular phylogeny (Jousselin et al. 2003) shed some doubt about the solidity of this classification. It disconnects species of subsection Urostigma from the rest of the subgenus and merge species of the subgenera Ficus, Sycidium, and Synoecia in the same cluster. All molecular studies, including that by Herre et al. (1996) indicate an isolated position of the neotropical section Pharmacosycea, as the sister-group of the rest of the genus.
DM. Berg, C.C. & X. Villavicencio, Taxonomic studies on Ficus (Moraceae) in the West Indies, extra-Amazonian Brazil, and Bolivia in Ilicifolia 5. 2004, DN. Berg, C.C. - Phytogeography, systematics and diversification of African Moraceae compared with those of other tropical areas in Chorology, taxonomy and ecology of the floras of Africa and Madagascar. 1998, DO. Berg, C.C. - Reproduction and evolution in Ficus (Moraceae): Traits connected with the adequate rearing of pollinators, in Modes of reproduction and evolution of woody Angiosperms in the tropics. 1989b, DP. Berg, C.C., Classification and distribution of Ficus in Experientia 45, DQ. Berg, C.C., Flora Malesiana precursor for the treatment of Moraceae 1: The main subdivision of Ficus: the subgenera in Blumea 48. 2003, DR. Berg, C.C., Subdivisions of Ficus subg. Urostigma sect. Galoglychia (Moraceae). in Proc. Kon. Ned. Akad. Wetensch. 89. 1986, DS. Carvajal, S. & L. K.-Shabes, Two new subsections of American species of the genus Ficus L. (Moraceae, subgenus Pharmacosycea Miq. sect. Pharmacosycea). in Bol. Inst. Bot. (Guadalajara) 6. 1998, DT. Corner, E.J.H., Check-list of Ficus in Asia and Australasia with keys to identification in Gard. Bull. Singapore 21. 1965, DU. Corner, E.J.H., Ficus in the Solomon Islands and its bearing on the Post-Jurasic history of Melanesia in Philos. Trans. 253. 1967, DV. Corner, E.J.H., Taxonomic notes on Ficus Linn., Asia and Australasia. V. Subgen. Ficus sect. Rhizocladus, Kalosyce, Sinosycidium, Adenosperma, and Neomorphe. in Gard. Bull. Singapore 18. 1960, DW. Diels, L., Die Moraceen von Papuasien. in Bot. Jahrb. Syst. 67. 1935, DX. Elmer, A.D.E., A fascicle of Sorsogon figs in Leafl. Philipp. Bot. 9. 1937, DY. Endlicher, S.L. in Gen. Pl. Suppl. 4. 1850, DZ. Gasparrini, G. - Nova genera, quae supper nonnullis Fici specibus struebat in Napoli. 1844, EA. Gasparrini, G. - Ricerche sulla natura del Caprifio, e del Ficus e sulla caprificazione in Napoli. 1845, EB. Herre, E.A., C.A. Machado, E. Bermingham, J.D. Nason, D.M. Windsor, S.S. McCafferty, W. van Houten & K. Bachmann, Molecular phylogenies of figs and their pollinator wasps in J. Biogeogr. 23. 1996, EC. Jousselin, E., J.-Y. Rasplus & F. Kjellberg, Convergence and coevolution in a mutualism: evidence from a molecular phylogeny of Ficus in Evolution 57. 2003, ED. King, G., The species of Ficus of the Indo- Malayan and Chinese countries in Ann. Roy. Bot. Gard. Calc. 1. 1887, EE. Mildbraed, J. & M. Burret, Die Afrikanischer Arten der Gattung Ficus in Bot. Jahrb. Syst. 46. 1911, EF. Miquel F.A.W., Annotationes de Ficus speciebus in Ann. Mus. Bot. Lugd.-Bat. 3. 1867, EG. Miquel, F.A.W., Prodromus monographiae Ficuum in London J. Bot. 6. 1847, EH. Ramirez B., W., A new classification of Ficus in Ann. Missouri Bot. Gard. 64. 1977, EI. Renner, O., Beiträge zur Anatomie und Systematik der Artocarpeen und Conocephaleen, insondere der Gattung Ficus in Bot. Jahrb. Syst. 39. 1907, EJ. Sata, T., A monographic study of the genus Ficus in Contr. Hort. Inst. Taihoku Imp. Univ. 32. 1944, EK. Weiblen, G.D., Phylogenetic relationships of functionally dioecious Ficus (Moraceae) based on ribosomal DNA sequences and morphology in Amer. J. Bot. 87. 2000, EL. in - undefined journal - 1. 1888, EM. in - undefined journal - 7. 1848

Uses

Formerly, in primitive societies, wild fig-plants had many uses and they have inherited many vernacular names: to modern man, the genus supplies the edible fig F. carica, a variety of ornamental plants, in the tropics and subtropics outdoors, in gardens, parks, and along avenues, and in colder parts of the world indoors. The Asian F. benjamina, F. elastica, and F. microcarpa are commercially the most valued species.
EN. Boer, E. & M.S.M. Sosef - Ficus in Plant Resources of South-East Asia. Timber trees: Lesser known timbers. 1998, EO. Brink, M., P.C.M. Jansen & C.H. Bosch, Plant Resources of South-East Asia 17 Fibre Plants. 2003, EP. Emeneau, M.B. in The strangling fig in sanskrit literature 13. 1949, EQ. Florence, J. in Flore de la Polynésie Française 1. 1997, ER. Fox, R.B., The Pinatubo Nigritos, their useful plants and material in culture in Philipp. J. Sci 81. 1952, ES. Minor species producing exudate, Ficus in Plant Resources of South-East Asia. 2000, ET. Plant Resources of South-East Asia 17 Fibre Plants. 2003, EU. Plants producing exudates but with other primary use, Ficus in Plant Resources of South-East Asia. 2000, EV. Rojo, J.P., F.C. Pitargue & M.S.M. Sosef - Ficus in Plant Resources of South-East Asia. 1999, EW. Tawan, C. - Ficus elastica in Plant Resources of South-East Asia. 2000, EX. Thomen, L.F., The latex of Ficus trees and derivatives as anthelmintics in Amer. J. Trop. Med. 19. 1939, EY. Van den Bergh, M.H. - Minor vegetables, Ficus in Plant Resources of South-East Asia. 1993, EZ. Viennot, O., Le cult de l’arbre dans l’Inde ancienne in Ann. Mus. Guimet 59. 1954

Citation

L. - in Gard. Bull. Singapore. 1965: (check-list)
L. - in Gard. Bull. Singapore. 1961: (addenda)
Miq. - in London J. Bot. 1848: (monogr.)
Miq. - in London J. Bot. 1847
L. - in Gard. Bull. Singapore. 1962: (addenda)
L. - in Ann. Mus. Bot. Lugd.-Bat. 1867: (list Old World spp.)
Corner - in J. Malayan Branch Roy. Asiat. Soc. 1933: (sect. Covellia & Neomorphe)
L. - in Blumea. 1975: (addenda)
Renner - in Bot. Jahrb. Syst. 1907: (anat.)
Gasp. - in Giorn. Bot. Ital. 1844
L. - in Gard. Bull. Singapore. 1960: (subg. Ficus, contnd.)
C.C. Berg - in Blumea. 2004
Diels - in Bot. Jahrb. Syst. 1935: (spp. papuan.)
Sata - in Contr. Hort. Inst. Taihoku Imp. Univ. 1944: (monogr.)
L. - in Gard. Bull. Singapore. 1939: (subg. Synoecia)
King - in Ann. Roy. Bot. Gard. Calc. 1887/1888: (monogr. Indo-Mal. spp.)
Elmer - in Leafl. Philipp. Bot. 1937
L. - in Blumea. 1970
Kochummen - in Gard. Bull. Singapore. 1998
L. - in Blumea. 1972
C.C. Berg - in Blumea. 2003
L., Sp. Pl. 1753: 1059
L. - in Gard. Bull. Singapore. 1960: (subg. Urostigma, Pharmacosycea & Ficus)