PROTECTION OF DEVELOPING SEEDS IN NEOTROPICAL ARACEAE

MICHAEL MADISON The Marie Selby Botanical Gardens, 800 S. Palm Ave., Sarasota, FL 33577

In flowering plants with ani­ When the fruit ripens mechanisms mal pollination and seed dispersal of attraction come into play once the reproductive cycle can be con­ more, including softening of the sidered to consist of four stages, re­ pericarp and production of colors presenting alternating phases of and fragrances. In a number of tro­ protection and display. In the pro­ pical genera, (e.g. Codonanthe, He­ tective phases immature flowers dychium, Marcgravia, Pittosporum, and fruits are safeguarded from Cariudovica, My ristica ) the pericarp predation and parasitism, while in breaks apart at maturity to reveal the display phases pollinators and the seeds with brightly colored arils dispersal vectors are attracted. or embedded in a juicy, colored pla­ This alternation of protection centa. and display is accomplished by a Since the adaptations for pro­ variety of mechanisms. Initially the tection of immature structures are developing flowers are protected by often contrary to the requirements bud scales, stipules, bracts, or the of the attractant phases, a delicate­ calyx and by cryptic coloration. As ly attuned sequence of developmen­ the flowers mature bud scales or tal events is required. Most studies stipules abscise and the pedicels or of reproductive biology have dealt peduncles elongate, elevating the exclusively with the attractive flowers to an exposed position. phases rather than considering the Heat, floral fragrances, and con­ cycle as a whole (e.g. Ridley 1930, spicuously colored bracts, perianth, van der Pijl 1969, Faegri and van or stamens may be elaborated; the der Pijl 1966, Proctor and Yeo effect of these in attracting pollina­ 1973), even though the adaptations tors may be enhanced by simultan­ of flowering plants to the protec­ eous deciduousness of the plant. tive phases are diverse and worthy Nectar or abundant pollen may be of study. A notable exception is the additional attractive factors. Fol­ investigations of Uhl and Moore lowing pollination is a second cryp­ (1973, 1977) which constitute a tic phase during which the develop­ superb study of protective mechan­ ing fruit is protected by abscision isms in the reproductive structures of showy perianth parts, by rapid of palms. formation of a hard pericarp, often In this paper I report observa­ cryptically colored, by accretion of tions on the reproductive cycles of the calyx or bracts, and/or by ela­ neotropical species of the family boration of chemical defenses. Araceae (philodendron family),

52 1979] MADISON: SEED PROTECTION 53 with special attention to the protec­ leaf-like, and in many species it tion of immature seeds. This fami­ serves only to protect the develop­ ly, with about 30 genera and 1200 ing spadix, becoming reflexed as species in the neotropics, forms a the spathe matures (Figure 1). conspicuous element of the vegeta­ However in some species, e.g. A. an­ tion in wet regions and includes dreanum, it is broad and brightly aquatics, terrestrial herbs, lianas colored and apparently plays a role and epiphytes. Except for a few re­ in pollination. In a group of species marks by Engler (1920) and Ridley allied to A. pedatum the spathe is (1930) hardly anything has been shaped like an inverted canoe with written about the fruits of aroids. the spadix pendent below (Figure The descriptions which follow are 2); in this case the spathe has ac­ based on observations of plants in quired the function of an unbrella. the wild made in the course of These species are native to very wet studies carried out since 1971 in middle elevation forests of the Central America and the Andes. western slopes of the Andes where One of the defining features there is a high probability of rain of the aroid family is the structure disturbing nectar or pollen. I have of the inflorescence, which consists observed Anthurium c.f. gualea­ of a spike of tiny flowers, termed num in Ecuador during a heavy the spadix, subtended by a large rain; the spadix, which was at an­ colored bract, the spathe. In all spe­ thesis, remained dry and was visited cies the spadix is protected before by flies, weevils, staphylinids, and anthesis by being tightly wrapped other insects. in the spathe, an additional layer of With the exception of the ge­ covering is provided by the sheath­ nus Spathicarga floral nectaries ing base of the subtending leaf or have not been reported for the Ara­ cataphyll. The initial phase comes ceae. However, copious production to an end with rapid elongation of by the pistils of stigmatic fluid, the peduncle and unfurling of the which is often, sweet to the taste, spathe to expose the spadix. From may to some · extent compensate this point a great diversity of flower­ for this deficiency. In Anthurium ing and fruiting mechanisms come stigmatic fluid is often abundantly into play, which are here described produced, and each flower elabor­ for each genus arranged according ates about the same amount (in to the subfamilial and generic classi­ contrast to Monstera where some fication of Engler (1920). flowers specialize as stigmatic fluid exuders). POTHOII)EAE The developing fruit in An­ thurium is protected by the cucul­ Anthurium: Anthurium in­ late tepals which almost entirely cludes about 600 species of terres­ cover it (Figures 3, 4). A layer of trial herbs, climbers, and epiphytes. sclereids below the epidermis pro­ The flowers are perfect and have vides a mechanical barrier around four tepals in two whorls of two; the berry. As the spadix ripens the the chief pollinators are flies, sphe­ berries soften and swell, and appar­ cid wasps, and the male euglossine ently increasing pressure in the spa­ bees. The spathe is usually flat and dix causes the berries, which abscise 54 AROIDEANA [Vol. 2 from the axis, to 'pop out' from bose or boat-shaped; the flowers are among the tepals (Figure 5). The perfect and lack a perianth, and are berries do not fall to the ground, pollinated by Trigona or related however, but dangle on four threads bees. Though nectaries are absent, representing part of the epidermis the basal flowers on the spadix are of the inner two tepals. These dang­ usually sterile and produce copious ling, brightly-colored berries, remi­ sweet stigmatic drops, apparently niscent of Magnolia seeds, are dis­ functioning as nectaries. persed by birds, as sometimes noted Since the perianth found in on herbarium specimens. Analysis Anthurium is lacking, the develop­ of stomach contents of Manacus ing seeds are protected by a differ­ manacus in western Ecuador showed ent mechanism. The stylar portion the birds to have been feeding heav­ of each ovary contains numerous ily on berries of Anthurium doli­ needle-like trichosclereids, all lying chostachyum (personal communi­ parallel to the axis of the flower cation from C. H. Dodson). (Figure 9). These tough needles, In some cases the popping out 1-2 mm long, form a considerable of the berries exposes a previously mechanical barrier around the de­ hidden bright color. For example, veloping seeds. At the time of ma­ in Anthurium buenaventurae the turity the fruit breaks in two trans­ developing spadix is dark purple, versely and the needle-bearing up­ including the tepals and protuber­ per portion falls away, reavealing ant apices of the berries. As the ber­ the seeds in a gray or brightly co­ ries are squeezed out from among lored pulp (Figure 10). The seeds the tepals the lower portion, which are picked off by birds. is bright yellow, becomes exposed, In Monstera punctulata the apparently signalling to dispersers protection of developing seeds pro­ that the fruits are ripe. vided by the trichosclereids is Heteropsis: I have observed augmented by a tough cap of iso­ fruits only of Heteropsis integerri­ diametric sclereids lying just below ma. The spathe abscises even before the epidermis of the ovary. Mon­ anthesis and the white spadix is stera obliqua lacks sclereids in the visited by bees and small hemiptera. fruit altogether, and also lacks the The developing fruit is green and abscission layer to discard the up­ the seeds are protected by a hard, per portion. This species has fruits sclerified pericarp. At maturity the which mature in only 6-8 weeks, pericarp softens and turns orange. while fruits of other species requrie The'musty-smelling fruits are borne up to 15 months (Madison 1977). at the ends of elongate hanging The lack of any apparent mechan­ branches, a situation suggestive of ism for protection of immature bat dispersal. fruits may be related to rapid ma­ turation. MONSTEROIDEAE Stenospermation: This genus Monstera; Monstera includes includes about 30 species of true about 25 species of scandent epi­ epiphytes with short stems and phytes, many of which have natur­ leathery leaves. The. floral structure ally perforated leaves. The spathe is very similar to that of Monstera, is white, yellow, or pink, and glo- and the globose spathe is deciduous 1979] MADISON: SEED PROTECTION 55 after anthesis. The developing seeds to the ground. This species is most are protected by needle-like tricho­ abundant along waterways, and sclereids in the apical region of the since the seeds float many of them ovary. At maturity the fruits turn may be water-dispersed (Bunting, yellow or orange and become soft. 1960). In addition, the swollen and The trichosclereids are not shed in juicy funiculus remains attached to a deciduous cap, as in Mons te ra, the seed, and this may serve as an but remain in the mature infructes­ elaiosome in dispersal by ants cence, which is pecked apart by which would find the seeds lying on birds or consumed by insects. the ground. Rhodospatha: Rhodospatha includes about 20 species of vines LASIOIDEAE in which the spadix is composed of Urospatha and Dracontium: perfect flowers lacking a perianth. Each of these genera includes about Pollination is similar to the preced­ a dozen species of tuberous herbs; ing two genera. Following anthesis both are fairly rare and poorly the spathe abscises and the develop­ known. The spadix consists of per­ ing fruits are protected by the fect flowers with a biseriate peri­ slightly hardened pericarp. The tri­ anth of 4-6 tepals. In Dracontium chosclereids found in the fruits of the spathe is usually dark purple Monstera and Stenospermation are and either sphaeroidally cucullate lacking. Predation of immature or spreading. The color and shape fruits of Rhodospatha in the wild of the spathe and its rotten-meat is not uncommon, and spadices of­ odor suggest fly or beetle pollina­ ten show signs of being gnawed on tion (Croat 1975) which is typical or burrowed in by beetles. At ma­ of the whole subfamily. In Uro­ turity the fruits soften and turn spatha the spathe is much longer white or pink. than the spadix and is often spirally Spathiphyllum: Spa thiphy l- twisted. Pollinators are unknown. lum includes about 40 species of In Urospatha, which often grows terrestrial herbs, mostly riparian. semi -aquatically in or along forest The spathe is white and broadly streams, the seeds have a corky epi­ boat-shaped. Pollination is chiefly dermis which makes them bouyant, by male euglossine bees attracted presumably an adaptation for water by floral fragrances (Williams and dispersal. Dressler 1976). The spathe is white at the time of flowering, and may The developing fruits are to turn green afterward. The spathe is some extent protected by the per­ persistent, often turning green and sisting spathe which loosely enve­ becoming, functionally, just another lops the spadix. The perianth and leaf. The developing seeds are pro­ hard pericarp also cover the seeds. tected by both a persistent peri­ The ripe fruits are colored berries anth, as in Anthurium, and by tri­ with one or a few highly sculptured chosclereids in the stylar portion of seeds, which are presumably dis­ the ovary, as in Monstera. persed by vertebrates. In the one At maturity the spadix breaks fruiting Dracontium which I have apart; the tepals may abscise and encountered in the wild the meter­ the ovary breaks irregularly in two. long peduncle had wilted and the In the Colombian species Spa thi­ beries were lying on the ground. phyllum floribundum the seeds fall 56 AROIDEANA [Vol. 2

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Figures 1-10. 1. Inflorescence of Anthurium buenaventurae. 2. Inflorescence of Anth­ urium pedatum, in which the spathe serves as an umbrella over the spadix. 3. Flower of Anthurium buenaventurae. 4. Same, in section, showing the ovary covered by the sclerefied tepals. 5. Ripe fruit of Anthurium buenaventurae, with the berries dangling from strips of the epidermis of the inner tepals. 6-10. Monstera tuberculata 6. Immature inflorescence wrapped in the leathery spathe. 7. Inflorescence at anthesis, the spathe open. 8. Flower. 9. Longitudinal section of the flower, showing trichosclereids in the upper part of the ovary. 10. Ripe fruit, the sclereid-containing part of the ovary falling away to expose the seed. 1979] MADISON: SEED PROTECTION 57

Montrichardia: Montrichardia the carpellate flowers are exposed. is a monotypica genus of semi-aqua­ Beetles or flies are attracted by tic herbs with fleshy erect stems to the fragrances, and in the case of 8 m tall, often forming dense stands P. bipinnatifidumand others, by along waterways. The spadix is di­ heat produced from uncoupled vided into a basal portion of car­ oxidation of starch (Nagy et al. pellate flowers lacking a perianth 1972). The spathe closes somewhat and an upper portion of staminate after the first night, but usually flowers. At anthesis the cream-co­ not enough to fully trap the in­ lored spathe opens slightly and an sects, as in some other aroids, intense sweet odor is emitted which e.g. Arum maculatum. Nonetheless, attracts various species of bees, pre­ dozens of beetles, especially rute­ sumably the pollinators. The spathe line scarabs, may be found of Montrichardia is deciduous after crammed in the lower chamber of anthesis and the developing fruits the spathe after the first night are protected by trichosclereids in of its opening. On the second the upper part of the ovary, as in night fragrances and heat are again Monstera. The mature berries are produced and pollen is shed. At yellow, about 4 cm long, and con­ this stage the stigmas are no longer tain abundant air-filled spongy tis­ receptive so that outcrossing is sue which aids in their flotation. insured. The ripe fruits abscise and fall into The beetles consume pollen the water which is the principal and large fleshy stigmas which means of dispersal. Ridley (1930) decompose to a slimy mass. How­ recounts observations of feeding on ever, if the beetles remain too long ripe Montrichardia fruits by the in the inflorescence they will Hoatzin (Opistocoma cristatus). also eat the flowers, which not infrequently happens. Two mech­ PHILODENDROIDEAE anisms serve to force the beetles from the inflorescence after polli­ Philodendron: Philodendron in­ nation. In a number of species cludes about 300 species of lianas the spath once again closes around and epiphytes. The flowers are the spadix, orientating itself so as naked and unisexual, with the car­ to fill up with rain water. In P. pellate flowers aggregated at the cruentospathum the inflorescence base of the spadix and the stamin­ sheds water at anthesis, but rotates ate flowers at the apex. In some 900 after flowering to become a cases these are separated by an water-holding structure (personal intervening zone of sterile stam­ communication from C.H.Dodson). inate flowers. The spathe usually Many other species when cut open shows a constriction part way are found to be full of water (e.g. up so that it forms two chambers, P. senatocarpium, P. karstenianum). the lower one enclosing the car­ The beetles are forced to leave the pellate flowers and the upper one inflorescence to avoid drowning. the staminate (Fig. 13). In Philodendron acuminatissi­ Pollination usually occurs on mum the spathe closes so tightly two subsequent nights. On the over the spadix after pollination first night the spathe unfurls and that the beetles are immobilized 58 AROIDEANA [Vol. 2 and may be crushed. Most escape beetles which are attracted by foul, before this stage, but the common or in a few cases sweet, odors. presence of holes in the lower Following pollination the spathe spathes indicates that beetles have once again wraps tightly around the had to chew through the tightening spadix, and serves to protect the spathe to make an escape. In this developing fruits from predation. species the spathe does not fill Generally the pollinators lay up with water. eggs among the Dieffenbachia The persistent leathery spathe flowers, which after anthesis protects the developing fruits after become immersed in slime from the anthesis. In most species it breaks disintegration of the large stigmas apart and is irregularly deciduous and accumulation of rain water. when the fruits mature. The aggre­ The larvae feed on the club-shaped gate of berries becomes colored, staminodia which surround each usually red or orange, and soft. ovary and which have a high The berries are eaten by birds and content of starch. Maturation of insects. I have observed beetles the flies apparently precedes mat­ and wasps crawling on the ripe uration of the berries; often tiny infructescences of Philodendron holes may be seen in the karstenaianum. They were consum­ spathe, presumably where adult ing the sweet juices of the pulpy flies (or beetles) have made their fruits and at the same time becom­ escape. With maturation of the ing covered with the tiny sticky fruits the spathe turns orange seeds, which weigh less than Img., and breaks apart. Its disintegration and which were apparently being is aided by the sharp backward dispersed by the insects. curvature of the spadix which In Philodendron senatocarpium occurs at this time. A double the spathe does not abscise at row of bright red berries is thus maturity but is persistent and turns exposed to the dispersing agents, a deep burnt orange color. On probably birds and small mammals. many of these the peduncle decays and the entire ripe infructescence falls to the ground. I have not COLOCASIOIDEAE observed how these are finally dispersed. Xanthosoma: Xanthosoma is a Dieffenbachia: Dieffenbachia in­ genus of about 50 species of cludes about 30 species of terrestri­ terrestrial herbs, many of them al herbs occurring in the dark massive 'elephant ear' plants with understory of wet forests, mostly at weedy habits. The spadices have lower elevations. The spathe is separate carpellate and staminate green and tightly wrapped around portions, the junction of which is the spadix, to which it is fused. indicated by a constriction in the The upper part of the spadix is spathe. The spathe unfurls at composed of staminate flowers anthesis and a profusion of insects and the lower part of carpellate visits the flowers, including hemi­ flowers surrounded by starch-filled ptera, trigonid bees, staphylinids, claviform staminodia. At anthesis weevils, and ruteline scarabs, the the spathe unfurls somewhat, last of which are the most likely allowing the entrance of flies or pollinators. 1979] MADISON: SEED PROTECTION 59

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Figures 11-16. 11. Carpellate flower of Dieffenbachia seguine, showing the ovary and two of the six staminodia. 12. Fruitng spadix of Dieffenbachia seguine; the curvature of the spadix helps to break away the brittle spathe, exposing the berries. 13. Inflorescence of Philodendron. 14. Developing fruit of Xanthosoma sagittifolium, the berries protected by the spathe. 15. Ripe fruit of Xanthosoma sagittifolium, the berries exposed. 16.Ripe fruit of Xanthosoma sp., the spathe splitting and reflexing to make a pseudo-flower.

After pollination the spathe destruction of developing fruits by closes and the lower portion may beetles is fairly common. fill with slimy water representing In most species of Xanthosoma accumulation of rain and disinte­ the staminate portion of the spadix gration of the stigmas. This is and upper part of the spathe apparently the same 'drowning' abscise or deliquesce soon after mechanism found in Philodendron anthesis. The lower part remains to get rid of potentially destructive erect and full of water for a time, pollinating beetles after anthesis. but soon droops to a pendent pos­ However, at least in X. sagittifolium ition. As the fruits mature the it does not seem to be as effective; remaining part of the spathe 60 AROIDEANA [Vol. 2 abscises, exposing ' the cream to DISCUSSION orange berries which become soft and juicy. In the neotropical species of In one unidentified species from Araceae at least nine distinct eastern Ecuador the spathe splits mechanisms are found for protect­ into five or six triangular segments ion of developing seeds: which become reflexed at maturity. 1) covering · of the fruits by ac­ These reveal a pink adaxial surface crescent . tepals with a sclerefied with brown markings, and the surface (Anthurium) infructescence constitutes a striking 2) hardening of the pericarp (Het­ 'pseudo-flower' (Fig. 23). eropsis) 3) changes of pericarp color from Syngonium: Syngonium in- white, yellow or orange to green cludes about 30 species of scandent after anthesis (many species) herbs and is primarily circum­ 4) surrounding the seeds with a Caribbean in distribution. The in­ barrier of needle-like trichoscler­ florescences are similar to Xan tho­ eids in the upper part of the ovary soma, but are often sweet-smelling (Monsteroideae, Montrichardia) and are probably pollinated by 5) rapid maturation (Monstera bees. Following anthesis the obliqua) upper part of the spathe and the 6) envelopment of the entire in­ staminate part of the spadix fructescence by a leathery spathe and the inflorescence becomes (Philodendroideae, Colocasioideae) pendent. The developing fruits are 7) orientation of the enveloping protected by the persistent envelop­ spathe to fill with rain water ing spathe, which is green. As the (Philodendron, Xanthosoma) berries mature they coalesce into a 8) distraction of potentially de­ soft syncarpium held together by a structive pollinator larvae by pro- ' brown skin. The spathe does not vision of starch-filled food bodies abscise at maturity but becomes (Dieffenbachia, Homalomena) red and serves as the attractive 9) presence of bundles of calcium part of the fruit. It is probably oxalate raphides in the unripe pecked apart by birds or other pericarp (all genera). vertebrates in search of the soft In most cases the function of sweet pericarp surrounding the these mechanisms is contrary to the seeds. In south Florida fruits of requirements of dispersal, so that naturalized Syngonium auritum are a corresponding array of adapt­ eaten by a variety of birds as atitons is required to reverse them well as squirrels. when the fruits ripen. Thus we Of the neotropical aroids Syn­ find extrusion of the berries from gonium exhibits the greatest devel­ among the tepals in Anthurium opmnet of the spathe which func­ shedding of trichosclereids in th~ tions sequentially in protection of Monsteroideae, and in many genera the immature inflorescence, pollina­ abscission of persistent spathes and tion, protection of developing softening and coloration of the fruits, and finally in dispersal. pericarp, often accompanied by production of fragrances and sugars. 1979] MADISON: SEED PROTECTION 61

Until recently investigations of Literature Cited the adaptive significance of repro­ Croat, T. B., 1975. A new species of ductive structures in tropical plants Dracontium (Araceae) from Panama. were greatly overshadowed by Selbyana 1 :168-171. morphological studies for strictly Engler, A., 1920. Araceae. Das Pflanzen­ taxonomic purposes. The expansion reich IV 23 A:1-71. of studies of pollination biology Faegrei, K., & L. vanderPijl, 1966. (e.g. vanderPijl and Dodson 1969, The principles of pollination ecology. Faegrei and vanderPijl 1966) and of Pergammon Press, Toronto, 248pp. fruit dispersal (e.g. vanderPijl1969) Madison, M., 1977. A revision of Mon-­ have stimulated a reexamination of tera (Araceae). Contr. from the Gray Herbarium of Harvard Univ. 207: reproductive structures from an 3-100. ecological point of view. These new Nagy, K.A., K. D. Odell, & R. S. Seymour studies have emphasized the phases 1972. Temperature regulation by the of reproduction in which animal inflorescence of Philodendron. Science agents are attracted to the plants. 178: 1195-1197. However, the attractant phases are Proctor, M., & P. Yeo, 1973. The pollina­ separated by an intervening period tion of flowers. Collins, London, in which protection of developing 418 pp. seeds and repulsion or evasion of Ridley, H. N., 1930. The dispersal of plants throughout the world. L. predators and parasites are primary Reeve & Co. Ashford, 744 pp. requirements. The wide variety of Uhl, N. H. & H. E. Moore, 1973. The mechanisms here reported for protection of pollen and ovules in the neotropical species of a single palms. Principes 17: 111-149. family, the Araceae, suggests that ------, 1977. Correlations adaptations to the cryptic phases of inflorescence, flower structure, may be quite diverse, and that and floral anatomy in some palms. investigation of this in other plant Biotropica 9:170-190. families will be worthwhile. vanderPijl, L., 1969. Principles of dispers­ al in higher plants. Springer-Verlag, Berlin. 153pp. vanderPijl, L., & C. H. Dodson, 1966. Orchid flowers, their pollination and evolution. Univ. of Miami Press, Miami, 214 pp. Acknowledgements: I wish to thank Williams, N. H. & R. Dressler, 1976. Dr. C. H. Dodson for contributing a Euglossine pollination of Spathi­ number of observations and suggestions phyllum (Araceae). Selbyana 1: 349- on this subject. 356.