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Selbyana 22(2): 197-2 12. 2001.

LIANASAND HEMIEPIPHYTES:DISTRIBUTION, DEVELOPMENT, AND ADAPTATIONS

Laboratoire de Botanique, UMR 5554, 163, me A. Broussonet, 34080 Montpellier, France. E-mail: [email protected]

Programme de modélisation des plantes, Cirad-amis B.P. 5035, 34032 Montpellier cedex 0 1, France. E-mail: caraglio @cirad.fr

ABSTRACT.Although poorly known and often neglected life forms, lianas and hemiepiphytes are frequently found in tropical canopies. Lianas (such as ) and hemiepiphytes (such as ) are specialized life forms of the that share a number of similarities, including spatial conditions and the requirement of a host . To better understand the biology of lianas and herniepiphytes, the authors, during a 15-year period (1985-2000), collected data to compare several aspects of these two groups: geographic and taxo- nomic repartition, seedling and establishment phases, architectural development, and vegetative propagation. Considering the prevalence of lianas and hemiepiphytes in tropical canopies, the authors discuss the re- sponse of these to environmental conditions and speculate on their role in forest dynamics.

Key words: ecology, growth strategy, hemiepiphyte, liana, plant architecture, taxonomic distribution

INTRODUCTION taken for a young , leading to errors in forest inventories (Caballé 1986, 1998). Many such er- In tropical forests, lianas generally are asso- rors stem from inadequate knowledge of the dif- ciated with more or less disturbed areas. Al- ferent ontogenetic stages of lianas and hemi- though hemiepiphytes may also be found grow- epiphytes. ing here, they are most frequent in undisturbed woody lianas and hemiepiphytes occupy a primary forest (Putz 1985, Balée & Campbell prominent place in forest ecosystems and may 1990, Hegarty & Caballé 1991, Phillips & Gen- reach over-al1 sizes and heights similar to can- try 1994, Pinard & Putz 1994). Liana and hemi- opy (putz 1995, Williams-Linera & Law- ePiphYte floristic &versiSr cari rePresent UP to ton 1995). To becorne established and grow in 20-25% of the vascular (Gentry & Dodson the canopy, lianas and hemiepiphytes use modes 1987, Gentry 1991). Their Presence and abun- of development net principally associated with dance cari reach sur~risingl~ Percentages: trees. In particular, the growth pattern of these up to 85% of forest trees can act as supports for organisms differs considerably from that of limas (Putz lg84a, Clark & Clark 1990, Camp- trees, and the properties of their specialized de- bel1 & Newber~ 19937 Pérez-Salicm~ 199817 velopment allow them to exploit the forest eco- and about 20% of forest trees have been reported system with considerable SuccesS. as colonized by hemiepiphytes (Prosperi 1998a). Increasingly limas and hemiepiphytes are in- The smdy of these specialized life fmms cari ~ludedin shdies of forest ecology and dynamics be difficult, and thus the growth of knowledge (Michaloud & Michaloud-Pelletier 1987, Law- relating to them has been harnpered. In the field, man & ~~dk~~~i1995, putz & Mooney 1991). limas and hemie~i~h~tesare net alwa~simme- Few in-depth studies, however, have been made diatel~recOgnizable in part or entirely; further, of the biology of lianas and hemiepiphytes, most in the canopy the^ may be integrated into tree contributions being limited to mention of their crowns. Recognition of a Young hemiepiphyfe in presence in floSstic treatments or as part of de- the canopy be very difficult and may require rnographic parameters in ecological sm&es. detailed observation. Similarly, depending on ~h~ objectives of study were to befter un- the develo~mentalstage? lianas or hemie~i~h~-derstand the special atVibutes that allow lianas tes m'Y be confUsed with 0th" biological types. and hemiepiphytes to evolve in the context of a In the understor~,the self-su~~oitingstage of a forest, as well as to begin to consmct hypoth- liana, as Hugonia (Linaceae), may be mis- eses regarding their respective roles in forest structure and dynamics. Our study compared * Corresponding author. geographical distribution and taxonomic repar- 197 198 SELBYANA Volume 22(2) 2001

tition and gathered new information regarding hills or mounds, paths and roads) provided un- their development of these forest canopy inhab- obstructed views. Occasionally, free climbing or itants. use of the Canopy Raft in French Guyana, Cam- eroon, and Gabon (Hallé & Pascal 199 1) were MATERIALAND METHODS necessary to gain access to tree canopies. . Drawing, an essential element of architectural We restrict our discussion to woody species analysis, permits the ordering and placing of of lianas and hemiepiphytes, as only these attain data into a coherent ensemble. Typically we the dimensions of large trees. We further define chose one or several informative angles of view. lianas as woody climbing plants that start their A rough draft captures the major features of the life on the ground, are not self-supporting except plant (e-g., , and forks, principal when young or facing a special constraint, and , or adventitious ), respecting perspec- whose reproductive phase occurs in sunlight. tive and proportion. Then a scheme, drawn using Woody hemiepiphytes are defined as plants that binoculars (10 x 40), figures al1 axes in the same begin their life on a tree and secondarily reach plane. Axes in front or in back of the plane are the ground by means of roots (Schimper 1888). not represented, or they are indicated showing We exclude plants of small stature such as Med- their insertion. Using a telescope, we then added inilla (Melastomataceae) or Zllia (). the final details (FIGURE1). The trait of beginning life in a tree also excludes plants named "secondary hemiepiphytes," such as Cyclanthaceae, , or some Ar- aceae (see Williams-Linera & Lawton 1995). Our data result from more than 15 years of Rooting in the soil is, for hemiepiphytes, a nec- field study (1985-2000) in the intertropical zone essary condition for development of sexual ma- of the Americas, Africa, and Asia. Work was turity and attainment of dimensions comparable conducted in al1 the major types to emergent trees. Characteristically, hemiepi- from dry forest to evergreen forest, and on con- phytes, from juvenile stages onward, express a tinents as well as islands (such as Mayotte and strongly developed adventitious root system. Comoros). The greatest portion of these field Previous architectural studies on lianas and studies was devoted to the study of lianas. hemiepiphytes have demonstrated that reitera- Geographic repartition and systematic value tion analysis provides the most relevant infor- were determined by a review of existing litera- mation for comparative studies between these ture. Taxonomic repartition was detennined by two life forms (Caballé 1986, Caraglio 1986, a review of existing literature corrected and en- Coudurier 1992, Delanoë 1992, Prosperi et al. hanced by the authors' field experience. 1995). Reiteration, the morphological process by which the plant reproduces in whole or in part its elementary architecture (Oldeman 1974, Bar- thélémy et al. 1989, Edelin 1991), is a phenom- Geographic Distribution enon essential to the construction of a . Reiteration allows a plant to conquer new spac- Lianas es, respond to local environmental conditions, In north temperate primary forests, such as in and ultimately exploit the canopy ( reiter- Poland, Germany, and France, large-diameter li- ation) and the soil (root reiteration). anas belonging to the genera () and Reiteration is called delayed or differed when (Ranonculaceae) are encountered, but it leads to duplication of the architectural unit their representation in these forests is low to by means of latent . Delay varies consid- moderate (Gentry 199 1). Southern temperate erably within a species and within an individual forests, notably the Valdivian forest, can be rel- in relation to the most recently formed growth atively rich in lianas; but the intertropical zone, units. Sprouts and suckers are exarnples of de- particularly evergreen forests have the greatest layed reiterated units. Sequential or immediate diversity of lianescent species (FIGURE2). The reiteration occurs concomitant with the process highest degree of diversity, recorded in South of tree development (Hallé & Ng 1981, Edelin America, may be attributable to the diversity of 1984) and normally leads to crown construction. the milieus in conjunction with geographic iso- Architectural analysis was conducted by ob- lation (Prance 1987, Gentry & Dodson 1987, serving living plants. For plants growing at soil Gentry 1991). C~nversely,the greatest number level to about a few meters high, direct obser- of individuals, or highest abundance, is found in vation was sufficient. For larger plants, binocu- Africa (Emmons & Gentry 1983, Caballé 1986, lars or a telescope were often necessary. Open Gentry 1993) and may relate to the paleoclimate sites in forests (e-g., tree-fa11 gap, forest edges, oscillation between hot and cold that took place FIGURE1. Illustration of different steps of architectural description. Different levels of simplification from a real plant to a schematic plant, here a Ficus nymphaeifolia (Moraceae, French Guyana). during the Quatemary Period (Lanfianchi & forests of New Zealand, especially certain spe- Schwartz 1990, Sayer et al. 1992, Maley 1996). cies of Metrosideros, Myrtaceae (Oliver 1930; Insufficient data on Asian lianas prevents an Dawson 1966, 1967). Highest species diversity evaluation of their repartition; however, Gentry is found in Asia, reflecting that the center of (1991) gives some numbers for Australasia (li- diversity for the genus Ficus (Moraceae) occurs anas + hemiepiphytes >2.5 cm), suggesting an here (Corner 1958, 1967) and that many Ficus abundance similar to that of the neotropics. species are herniepiphytes.

Hemiepiphytes Taxonomie Distribution Essentially inhabitants of tropical hurnid for- est canopies (FIGURE3), from sea level to 2500 One measure of success for a plant group's m altitude (Williams-Linera & Lawton 1995), growth strategy is the group's importance in the hemiepiphytes also may be found in temperate colonized habitat; another is reflected in the de-

FIGURE2. Geographic distribution of lianas. SELBYANA Volume 22(2) 2001

FIGURE3. Geographic distribution of hemiepiphytes. gree of species diversity. Many liana and hemi- a very large genus (300 spp.), is in a liana-rich epiphyte families demonstrate these growth (FIGURE6). strategies, but we consider only the major taxa at the family and genus levels. Hemiepiphytes The leading families with hemiepiphytes are Lianas Araliaceae, Cecropiaceae, Clusiaceae, Melasto- The family with the largest number of liana mataceae, and Moraceae (FIGURE7). Unlike li- species is Leguminosae with Ca. 1100 spp., fol- anas, a single family, Moraceae, predominates, lowed by Asclepiadaceae, , Mal- and this by virtue of a single genus, Ficus, with phighiaceae, , , and about 500 species (FIGURE8). Clusia (Clusi- Hippocrateaceae (FIGURE4). Typically Hippo- aceae) ranks second in terms of numbers with crateaceae, Passifloraceae, Dichapetalaceae, and about 85 species (FIGURE9). Bignoniaceae display a lianescent and have In surnmary, lianas evidently have a broader a high percentage of liana species (71%, 68%, geographic repartition than hemiepiphytes pri- 58%, and 50% respectively; FIGURE5). Overall, marily because of their presence in northern and about 30 families are rich in lianas (30% lianes- southem temperate zones. Notwithstanding, it is cent spp.). The palm family (), com- in the inter-tropical zone that the two life forms paratively poor in lianas (20% of its spp.), con- achieve their greatest expression. tains (rattans), the largest genus of li- A large disparity exists in terms of species mas (350 spp.). PassiJora (Passifloraceae), also numbers between hemiepiphytes and lianas. Al- though different authors (see Gentry 1993) agree on a total of 20,000 climbers (including , Passifloraceae lianas, and some hemiepiphytes), only 6000 are woody lianas, and woody hemiepiphytes number only 850 (TABLES1, 2). A large number of an- giosperm families have woody lianas (5 l), com- pared with the 28 families having woody hemi- epiphytes. Although a single family, Moraceae, predominates among hemiepiphytes, several families have significant numbers of liana spe- cies. Conifers (Pinopsida) have no lianas or hemiepiphytes; but at a higher , such as , lianas are present in the genus (Gnetaceae), and Gnetaceae is primarily a lianescent family. No hemiepiphytic 51 famiiies - 6000 spp. gyrnnosperms have been found. Among mono- FIGURE4. The most species-rich families of lianas. cotyledonous angiosperms, besides the rattans Hipp Pass Dich Bign Aris Ascl Malp Apo Arec Leg

RGW 5. Liana families, with number of lianescent species as a percentage of the total species. Apo = Apocynaceae; Arec = Arecaceae; Aris = ; Ascl = Asclepiadaceae; Bign = Bignoniaceae; Dich = Dichapetalaceae; Hipp = Hippocrateaceae; Leg = Leguminosae; Malp = Malpighiaceae; Pass = Passiflora- ceae; Sap = .

previously mentioned (Calamus, Arecaceae, and seedling is small, develops a primary root sys- some other genera), the genus Freycinetia (Pan- tem, and grows slowly at this stage. The primary danaceae) with about 175 species is exclusively root system is ephemeral but assures the nutri- lianescent. In the , the large genus Phil- tion and attachent, often in precarious posi- odendron (ca. 300 spp.) harbors the only mono- tions, of the seedling. cotyledonous hemiepiphytes (ca. 130 spp.). Soon after the primary root system is elabo- rated, the seedling searches for the earth by Life History means of a highly developed, rapidly growing adventitious root system (FIGURE10C). Once Lianas are plants that germinate in the earth. contact is made with the soil, upward growth of When Young, they are self-supporting, and their the shoot system into the canopy begins (FIGURE growth is relatively slow. A "search-for-sup- 10D). Rapid elaboration of the root system by port" phase is crucial for shoot establishment. reiteration also occurs, leading to the expansion Upon contact with a support, the plant under- and complete expression of the root and shoot goes an anatomical transformation associated systems, without necessarily being in full Sun- with development of a host attachment system light. This is followed by flowering and fruiting (FIGURE1 OA). (FIGURE10E). Hemiepiphytes range in length Conversely, ascendance toward and into the from a few to 40 m. canopy represents a period of rapid growth, but one with many "peaks" (e.g., Tetracera alni- Architecture folia, ; Caballé 1980). Expansion and complete expression of the plant body in full Crown construction sunlight is followed by the reproductive phase Lianas grow essentially by relay; that is, one with flowering and fruiting (FIGURE10B). module develops, the extremity dies, and anoth- In parallel with host attachment and ascen- er module takes over. According to Coudurier dance, a liana develops an adventitious root sys- (1992), a typical liana module is made up of a tem that primarily performs a nutritional func- dominant primary mis, the trunk, and reduced tion, rarely an attachment one. Host attachment axillary formations. The principal axis can be is usually by means of shoot modifications. In either orthotropic with a twining or tendrilled this manner, limas, such as the genus distal portion or a mixed axis that is orthotropic (Mimosaceae), can achieve sizes of 10-100 m, proximally and plagiotropic distally. At the sum- even up to 1 km long and more! Hemiepiphytes mit of the trunk, one or two reiterated complexes genninate on an aerial support. The resultant form, which will reiterate at their summit. The

Calamus Passiflora Combretum Serjania Uvaria FIGURE6. Liana genera, with bars representing the percentage of liana species in the farnily. SELBYANA Volume 22(2) 2001

Oîhers

Moraceae Mora Cec Aral Clu Mela FIGURE8. Importance of hemiepiphytes, with number of hemiepiphyte species as a percentage of the total species. Note: Mora = Moraceae; Cec = Cecro- viaceae; Aral = Araliaceae; Clu = Clusiaceae; Mela = Melastomaceae.

32 famiiies - 850 spp. FIGURE7. The most species-rich farnilies of herni- epiphytes.

TABLE1. Families and genera including woody herniepiphytes.

No. hemi- Total spp. Family epiphytic spp. in family Woody hemiepiphyte genera Aquifoliaceae 1 420 Zlex Araceae 133 2950 Philodendron Anacardiaceae 3 850 Rhus, Spondias Araliaceae 77 800 Brassaiopsis, Pentapanax, Oreopanax, Polyscias, Pseudopanax, SchefJZera Bignoniaceae 2 725 Schlegelia Bombacaceae 4 250 Ceiba (syn. Spirotheca) Burseraceae 1 540 Bursera Cecropiaceae 45 200 Coussapoa, Poikilospermum Celastraceae 2 1000 Clusiaceae 95 1350 Clusia, Clusiella, Havetiopsis, Odematopus, Quapoya, Renggeria Cornaceae 3 90 Griselinia Cunoniaceae 3 340 Ackama Weinmannia Epacridaceae 1 400 Dracophyllum Ericaceae ? 3350 Cavendishia, Disterigma, Gaultheria, Gonocalyx, Rhododendron, Sphyrospemum, Vaccinium, Disterigma 20 600 Melastomaceae 88 4750 Adelobotrys, Bertolonia, Blakea, Dalenia, Dissochaeta, , Miconia, Omphalopus, Topobea Moraceae 500 1200 Ficus Myrsinaceae ? 1250 Cybianthus, Embelia, Grammadenia, Rapanea Myrtaceae ? 3850 Metrosideros Onagraceae ? 650 Fuchsia 1 240 Pittosporum Rosaceae 3 3100 Pyrus Rubiaceae ? 10,400 Coprosma, Cosmibuena, , Posoqueria, Schradera, Tirnonius ? 1700 Zanthoxylum Sapotaceae ? 1100 Sideroxylon ? 2600 Markea 1 1900 Premna ? 830 Melicytus Ficus Clusia Blakea Coussapoa FIGURE9. Hemiepiphyte genera, with bars representing the percentage of hemiepiphyte species in the family.

crown of a liana that reaches the canopy is thus Alternately, in some species of Clusia, as well formed of modules or superposed reiterated as Coussapoa angustifolia, C. latifolia (Cecro- complexes (FIGURE11). The tmnk or base has piaceae), Dendropanax spp. (Araliaceae), Ficus large dimensions, and the crown is made up of guianensis and F. leiophylla (Moraceae), reiter- progressively smaller units. Transformation to ation is known to lead to a completely different the lianescent life style-passage from a self- occupation of space. Little growth of the trunk supporting to non-self-supporting adult-is ac- is accompanied by considerable basal reitera- companied by a number of remarkable and well- tion. Such plants develop completely in the heart known architectural and anatomical modifica- of the host tree's crown, competing with the sup- tions, collectively referred to as metamorphosis. port branches for light. Sequential basal reiter- Caballé (1993) wrote, "the aerial architecture ation, apparently a property offsetting this in- and its development are directly affected by this convenience, is the source of ramified groups of change of state: growth is accelerated, inter- reiterated complexes that intercalate between the nodes are elongated, climbing structures or support branches. These groups are (1) either mechanisms are established, the shape of vertical ones such as in Coussapoa, where al1 may be transformed completely and they can be reiterated complexes are vertical and which arranged differently as phyllotaxy and branching eventually can reach the top of the host crown characteristics are modified . . . (Prévost 1967, (Caraglio in press); or (2) more of less horizon- Cremers 1973, 1974, Huc 1975, Givnish & Ver- tal ones as in Ficus, wherein the reiterated com- meij 1976, French 1977, Etifier 1981, Blanc & plexes fan out from the base into the available Andraos 1983, Pefialosa 1983)." space. This mode of reiteration leads to a - Despite numerous and varied morpho-ana- like habit (Caraglio 1986). tomical changes during liana development, over- Lastly, hemiepiphytic species such as Blakea al1 crown construction is relatively uniform sp. (Melastomataceae) and Clusia cuneata (Clu- compared to that of hemiepiphytes. siaceae) exhibit a third and most original manner Crown construction in hemiepiphytes primar- of occupying space in the host. Self-supporting ily results from the modalities of sequential re- duplicated modules develop from the typically iteration (Prosperi et al. 1995). construction, short tnink. Once these modules reach about 3- which has an essential role in hemiepiphyte and 4 m and begin to get heavy, their self-supporting host tree relations, determines the extension and ability is compromised. This results in a sinuous form of the crown with which the hemiepiphyte trajectory wherein the long non-supporting mod- will CO-habit the support tree. We recognize ules multiply their points of attachment on the three types of hemiepiphytic habit: arborescent, supporting branches of the host. Each reiterated shmbby, and lianescent (FIGURE12). complex grows up between openings in the In species that present a single well-developed crown branches and, in this manner, makes up trunk with long, simple lateral branches, reiter- part of a fragmented crown. This mode of reit- ation only serves to reinforce the basic architec- eration recalls the strategy of lianas when they tural unit by developing supplementary axes in pass from the juvenile to adult stage (Coudurier the crown periphery. The reiterative process also 1992, Delanoë 1992). favors the horizontal spreading and extension of the hemiepiphyte, allowing it to grow above the Vegetative propagation crown of the support tree (e.g., Clusia rosea, Vegetative propagation in lianas essentially Clusiaceae; Ficus nymphaeifolia, Moraceae). concerns the shoot system (FIGURE13A). Al1 Such an essential apical growth confers to these known modalities of vegetative propagation are hemiepiphytes an arborescent habit. expressed in lianas at different times during their 204 SELBYANA Volume 22(2) 2001

TABLE2. Families and principal genera of woody limas.

No. liana Family SPP. Total spp./family Principal woody liana genera - - - Actinidiaceae Actinidia Anacardiaceae Rhus Artabotrys, Friesodielsia, Monanthotaxis, Popowia, Uvaria Apocynaceae Forsteronia, Mandevilla, Landolphia, Melodinus, Odontadenia, Prestonia, Araceae Monstera, Philodendron Araliaceae SchefJEera Arecaceae Calamus, Daemonorops, Desmoncus Aristolochiaceae Asclepiadaceae Asclepias, Cecropegia, Gonolobus, Hoya, Oxypetalum, Secamone Asteraceae Gynura, Mikania, Montanoa, Mutisia, Senecio Bignoniaceae Adenocalymna, Anemopaegma, Arrabidaea, Memora Caesalpiniaceae , Caesalpinia Capparidaceae Caprifoliaceae Lonicera Celastraceae Loeseneriella, Tontelea Combretum Agelaea, Cnestis, Connarus, Rourea Convolvulaceae Convolvulus, , Merremia Cayaponia, Cucurbita, Gurania, Momordica Dichapetalaceae Dilleniaceae Hibbertia, Davilla, Doliocarpus, Tetracera Ephedraceae Ephedra Euphorbiaceae Croton, Dalechampia, Macaranga, Phyllanthus, Tragia, Alchornea Gnetaceae Gnetum Illigera Hippocrateaceae Hippocratea, Salacia Hydrangeaceae Iodes Linaceae Hugonia Loganiaceae Malpighiaceae Heteropterys, Banisteriopsis, Hiraea, Mascagnia, Stigmaphyllon, Tetrapterys Melastomataceae Gravesia Mendonciaceae Menispermaceae Abuta, Cissampelos, Stephania, Tilacora, Tinaspora Mimosaceae , Mimosa, Entada Jasminum Freycinetia Papilionaceae Dalbergia, Lonchocarpus, Machaerium, Millettia, Rhynchosia, Canavalia, Centrosema, Clitoris, Dioclea, Passifloraceae Passijlora, Polygonaceae Ranunculaceae Clematis , Rosaceae Rosa, Rubus Rubiaceae Canthium, ~anettia,Mussaenda, Randia, Sabicea, Tarenna, TABLE2. Continued.

No. liana Family SPP. Total spp./family Principal woody liana genera Rutaceae ? 1700 Zanthoxylum Sapindaceae 400 1350 , Serjania Schisandraceae ? 47 Schisandra ? 225 Solanaceae 80 2600 Solanum Verbenaceae 120 1900 Aegiphila, , Vitex, Vitaceae 400 800 Cissus, Vitis

life (Beekman 1981, Caballé 1994). Lianas ex- the appearance of sprouts at the base of the hibit terrestrial and aerial layering, transversal plant, development of a horizontal and/ and longitudinal shoot fragmentation, , or its dipping to the ground, and capacity to re- flagella, basal shoot sprouts, and lignotuber for- iterate and thereby form a new organism at a mation. distance from the parent plant. According to The lianescent habit could not be achieved Coudurier, "the result of this tendency is the re- without a series of attachent points along one alization of horizontal structures of great size or more supports (Coudurier 1992, Putz 1995). that permit vegetative multiplication at a dis- If the extremity of a growing liana in the un- tance." Araceae and Piperaceae lianas have spe- derstory does not have a support, the shoot will cialized structures known as flagellas, which are touch the soil. The portion of the shoot in con- very effective at propagating vegetatively. Fla- tact with the soil can continue to grow, root, gellas result from morphological transformation ramify, and even split up. Over time, such lay- of growing shoot apices; for example, an inflo- ering is followed by splitting up of the shoot that rescence (reproductive shoot) may be replaced leads to creation of new individuals or ramets by a vegetative shoot such as a branch. As Blanc (i.e., Tetracera alnifolia, Vitaceae, in Gabon; (1980) explained "the effect of a flagella is to Caballé 1980). convert the apical to a branch, and rep- Longitudinal fissuring of the stem of adult li- resents an exploration strategy and a method of anas is cornmon in several different families. defense for the plant in ecologically limited con- Specific species that split in this manner include ditions." Flagellas correspond to occasional Dalhousiea africana (), Cissus dinkla- methods of vegetative multiplication, whereas gei (Vitaceae), Combretum mortehanii (Combre- stolons are a normal part of the differentiation taceae), Landolphia sp. (Apocynaceae), Loese- of a lianescent plant. neriella clematoides (Hippocrateaceae), and Studies conducted on Entada scelerata (Mi- Millettia sp. (Fabaceae) (Caballé 1994). In these mosaceae) in Gabonese forests have demonstrat- plants, the whole anatomical structure of the ed that it reproduces vegetatively by very par- shoot prefigures the cleavage lines, and hence ticular mechanisms (Caballé 1977). At a late the longitudinal fissures that lead to clone for- stage in the life of the liana, the main shoot in mation. contact with the soil develops a structure sirnilar The biological significance of forma- to the parent root collar, forming a relay link at tion by lianas is rarely discussed (Blanc & An- a dozen meters from the initial site of germina- draos 1983). A stolon, a shoot that develops tion of the parent trunk. Gradually, the shoot from an axillary meristem and grows horizon- segment between the parent and relay root col- tally along the ground, is often confused with lars degenerates, and the new root collar ("re- organic understory debris. Liana stolons exhibit placement collar") assumes the function of the long slender intemodes and rarely, petiolate parent collar. The shoot developing from the re- leaves. Stolons have the capacity to form adven- placement collar represents a new, young struc- titious roots and to reiterate the young plant's ture, which consequently undergoes total reiter- shoot structure (e.g., Arrabidaea inaequalis, ation. Development of a second root collar en- Bignoniaceae; Doliocarpus spp., Dilleniaceae; ables the resultant clone to explore and exploit Pacouria guianensis, Apocynaceae; Solanum the forest environment at a distance of 12 m terminale, Solanaceae). In French Guiana, Cou- from the parent plant. durier (1992) concluded that their different To establish themselves and survive in an un- modes of represented stable milieu such as the canopy, herniepiphytes intermediary evolutionary steps toward stolon have developed an opportunistic life style that formation. He recognized the following steps: essentially depends upon their capaciîy to prop- 206 SELBYANA Volume 22(2 ?O(:) l agate vegetatively (Pr6speri 1998b). This capac- ity is expressed in the formation of suckers, which occur with great frequency in the genus Coussapoa (Cecropiaceae), and layering, found in some Clusia (Clusiaceae) and widespread in Ficus (Moraceae). In Coussapoa latifolia, suck- ers develop dong the principal or "tape" root (FIGURE13B), which links the hemiepiphyte to the soil; in C. asperifolia, they develop from an- chorage roots of the tape root. In Clusia rosea, suckers develop from aerial roots of basal branches and, at the soil level, emanate from the soil surface, spreading laterals of the tape root. With an organization similar to that of the parent plant, these suckers guard an autonomous char- acter following fragmentation of the root from which they arose and development of their own adventitious root system, which provides an- chorage, nourishment, and tape roots. RGURE11. Crown building in Passifloraceae (from Layering in hemiepiphytes can be produced Delanoë 1992). in the canopy or on the ground. In Clusia cu- neata and Ficus amazonica observed in French Guiana and Blakea sp. and Ficus maitin studied es (Poaceae) wherein the central portion dies, in Venezuela, layering occurs upon contact of and the colony fragments and colonizes areas at certain branches of the hemiepiphyte with those a distance from the original site of parent - of the support (Caraglio 1985, Pr6speri 1998a). ling and establishment. Such layering allows these species to gradually colonize the crown of their host by means of DISCUSSIONAND CONCLUSIONS multiple anchorage points. In C. rosea, layering begins with formation of large tape roots that, The two biological types, lianas and herni- upon reaching the soil, assure the direct nutrition epiphytes, can be separated on the basis of sev- of the axis from which they derive. These roots eral criteria (TABLE3). An analysis of their de- are located on the proximal ventral portion of velopment, particularly the manner of crown the lower branches and have a diameter similar construction and vegetative propagation, indi- to those of the trunk. They constitute root col- cates that the process of reiteration is of major urnns similar to the pillar roots of Banyan trees adaptive importance to these plants as they com- (such as Ficus benghalensis). Distal to the pillar, pete for available space and to their survival in the branch augments in diameter and grows pro- the forest. In a general way, sequential reitera- gressively upright until it constitutes a reiterated tion takes over in canopy expansion and explo- complex. In addition, the region between the ration, whereas delayed reiteration comes into branch proximal to the pillar and its insertion on play in the survival of the organism as well as the trunk forms a reiterate, ultimately becorning in its renewal (e-g., of damaged or destroyed autonomous from the mother plant by gradua1 parts). degeneration of the point of contact. In this way, For lianas, reiteration allows the plant to go a new individual is produced. This habit recalls through the difficult passages in the understory a sirnilar phenomenon well-known in tuft grass- and then to explore the canopy by successive

FIGURE10. A, B. Lianas seen from the canopy and understory. A. Connaraceae liana and support tree, evergreen forest, Kouyi, Congo (Photos G. Caballé). B. Combretum (Combretaceae) liana in , evergreen forest, Bélinga, Gabon. C-E. Hemiepiphytes as seen from the canopy and understory. C. Evergreen forest of French Guiana, profile showing a Clusia (Clusiaceae) growing on a host tree. The upper arrow indicates part of the Clusia crown and the lower arrow a large root encircling the support tree's trunk (Photo Y. Caraglio). D. Clusia platystigma (Clusiaceae) hemiepiphyte in evergreen forest, St. Elie, French Guiana; the arrow indicates Clusia branches with large shiny leaves are intercalated into those of the support tree (Photo Y. Caraglio). E. Two individuals of Clusia sp. (Clusiaceae) Creek Voltaire, French Guiana. The arrow at left indicates a part of the crown imbricated in that of the support tree; the arrow at right indicates the tape root and anchorage roots (Photo E Hallé). SELBYANA Volume 22(2) 2001

F'IGURE12. Crown building in hemiepiphytes. The young individual (upper left) can become a tree (upper nght), a shnib (below left), or a liana-like plant (below right).

placement of reiterated complexes. Competition Lianas and herniepiphytes have developed a between a hemiepiphyte and its support also de- cornrnon "opportunistic" strategy based essen- pends directly on its ability to reiterate. Depend- tially upon their compartmentalization in forests. ing upon their developmental potentials and op- Their highly developed capacity to produce ad- portunities in the canopy, hemiepiphytes occupy ventitious roots make possible a strategy, which, different volumes. When taking an arborescent in turn, enables ensuing structures such as form, the crown of the hemiepiphyte is more or sprouts and layers to become autonomous indi- less compact and can dominate that of the sup- viduals and, hence, clones. L port. Shrubby or lianescent hemiepiphytes have Clona1 growth is for hemiepiphytes and limas a "discontinued crown" that is capable of inter- an adaptive process essential to their survival calating between the support branches and oc- because their habitat is precarious and depends cupying the available space at the interior or pe- upon the stability of the support tree(s) and/or riphery of the host tree's crown. the forest structure. FIGURE13. Vegetative propagation. A. Liana Bauhinia (Caesalpiniaceae), longitudinal fissuring of shoot, evergreen forest, St. Elie, French Guiana (Photo G. Caballé). B. Herniepiphyte suckers developing from tape root of Coussapoa latifolia (Cecropiaceae), evergreen forest, St. Elie, French Guiana (Photo J. Pr6speri).

TABLE3. Main characteristics of woody lianas and hemiepiphytes.

Characteristics Lianas Hemiepiphytes Taxonornic 51 farnilies 28 farnilies distribution Geographic Pantropic and temperate areas Pantropics distribution Development Terrestrial germination Epiphytic germination Installation phase of shoot system Installation phase of root system Anchorage by leafy parts Anchorage by adventitious roots Crown building by stems stacking Edification by stems stacking Not self-supporting except some juvenile Not self-supporting except some adult stages stages Vegetative propagation: Stem Vegetative propagation: Root and stem Ecology Reaching canopy from understory Reaching canopy from lower canopy High response to environmental factors High response to environmental factors Disturbed areas Stabilized areas Tree-fa11 gap, forest border, river edge Branch-fa11 gap, tree crown Pioneers Pioneers 210 SELBYANA Volume 22(2) 2001

point out new ideas about growth habit evolu- tion (i.e., trees versus lianas; see Putz 1980). An overall perspective of their biology should take into account aspects of ecophysiology (Hol- brook & Putz 1996). 6

t The authors thank Dawn Frame for her very helpful translation of the paper. This is publi- cation No. ISEM 99-1 10 of Institut des Sciences de l'Evolution, UMR 5554 du CNRS.

FIGURE 14. Forest profile showing how lianas and herniepiphytes integrate into forest gaps such as this tree-fa11 gap, with lianas in gray (above), and hemi- epiphytes in black (below). Baleée, W. and D.G. Campbell. 1990. Evidence for the successional status of liana forest (Xingu river ba- sin, Amazonian Brazil). Biotropica 22(1): 36-47. Barthélémy, D., C. Edelin and E Hallé. 1989. Archi- tectural concepts for tropical trees. Pp. 89-100 in Their different growth strategies, and espe- L.B. Holm-Nielsen., I.C. Holm-Nielsen and H. cially vegetative multiplication, are a response Baslev, eds. Tropical Forests. Botanical Dynam- to more or less violent environmental changes. ics, Speciation and Diversity. Academic Press, Their capacity for growth (extension of lianas to London. reach light, adventitious rooting of herniepi- Beekman, E 1981. Structural and Dynamic Aspects of phytes to ensure survival) pennits them to rap- the Occurrence and Development of Lianas in the idly exploit free spaces. Their capacity to re- Tropical Rain Forest. Agricultural University, De- spond to light stimulation enables them to pro- partment of , Wageningen. Blanc, P. 1980. Observations sur les flagelles des Ar- gress through the forest. In the elaboration of aceae. Adansonia 20(3): 325-338. their architecture (competition between host and Blanc, P. and K. Andraos. 1983. Remarques sur la dy- hemiepiphyte crowns and, for lianas, passage namique de croissance dans le genre L. (Pi- through different forest strata), response to light peraceae) et les genres affines. Adansonia 3: 259- confers upon them a remarkable capacity to 282. adapt to even strong variations in the forest eco- Caballé, G. 1977. Multiplication végétative en forêt system. dense du Gabon de la liane Entada scelerata (Mi- Lianas cornmonly occupy fragmented and dis- mosoïdeae). 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