Flower Food Tissues As Reward for Pollinating Birds

ISSN 0373-580 X Bol. Soc. Argent. Bot. 37 (1-2): 71 - 77. 2002

FLOWER FOOD TISSUES AS REWARD FOR POLLINATING BIRDS

G. G. ROITMAN' 3, A. N. SÉRSIC23, A. A. COCUCCI2 and N. H. MONTALDO1

Summary: Nectar is the reward regularly offered by flowers to their pollinating birds. Studies on pollination by birds have focused on nectar as a reward while alternative reward systems have been poorly studied. Previous reviews have shown the presence of food tissues that serve as nutritive rewards to different classes of pollinators. However, in a recent revision of plant-bird interactions, the existence of a solid reward for birds has been disregarded. In South America at least three cases of this very particular bird-flower Interaction have been recently studied. In this paper we describe the syndrome features (flower morphology, reward properties, position of the pollination unit, flower color display and common visitors), that deviate from the typical ornithophilous syndrome, and its possible origin is discussed. Key words: Flower, food reward, pollination, birds, syndrome, review.

Resumen: Tejidos alimenticios florales como recompensa para las aves polinizadoras. El néctar es la recompensa típica que las flores ofrecen a las aves polinizadoras. Los estudios sobre ornitofilia se han concentrado en el néctar como recompensa, mientras que otras retribuciones alternativas fueron esca¬ samente analizadas. Revisiones previas han mostrado que la producción de tejidos alimenticios puede servir como recompensa para diferentes polinizadores, y al menos tres casos de esta particular interacción se estudiaron últimamente en América del Sur. Sin embargo, una revisión reciente sobre interacciones planta-ave descarta la presencia de recompensas sólidas. En este trabajo describimos las caracterís¬ ticas del síndrome que lo diferencian del típico síndrome ornitófllo (morfología floral, propiedades de la recompensa, posición de la unidad de polinización, color de la exhibición floral y visitantes más comu¬ nes), y también discutimos su posible origen. Palabras clave: Flor, alimento como recompensa, polinización, aves, síndrome, revisión

INTRODUCTION the most commonly found tubular,bilabiate or brush- type architectures are related respectively to modes Nectar is the reward(primary attractant) regularly of pollen placement on the back, the front of the offered by flowers to their pollinating birds. In bird- head and the ventral body parts (Feinsinger, 1991). flowersitspresence is announcedexclusively by color (secondary attractant), which is often vivid and not Nectar-feeding birds infrequently scarlet red. Such announcement may enable the birds to locate and individualize particular Around the world nearly twelve families ofbirds types of flower among many others. are known as flower visitors (Armstrong, 1979; Flower parts have mechanical functions normally Stiles, 1981; Westerkamp, 1990). In the Neotropics, involved either in adaptation to the structure and the most notorious bird pollinators are Trochilidae. behavior of the birds or in the deterring of pollina¬ (hummingbirds). This family of 300 species hum¬ tors other than birds. Such is the case of pendant mingbirds,is considered the largest andmost highly inflorescences (coupled with capillary devices to specialized group of flower-feeding birds (Stiles, avoid the dripping of nectar), mechanical deterrents 1981). Passerine pollination has been considered a (strong corollas), morphologies adjusted to ensure very common interaction in the Old World (Faegri pollen placement on different parts of the bird’s & van der Pijl, 1979), but in the Neotropics the im¬ body, etc (Faegri & van der Pijl, 1979). For example, portance of birds other than hummingbirds as pol¬ linators has been stressed As an ex¬ 1 only recently. Laboratorios de Botánica “L. R. Parodi”, Cátedra de Bo¬ ample at least 17 species of the Neotropical tánica Agrícola. Facultad de Agronomía de la Universidad Erythrina (Fabaceae) show adaptations to pollina¬ de Buenos Aires. Av. San Martín 4453, RA-1417 Buenos Aires, Argentina. tion by perchingbirds (Bruneau, 1997; Steiner, 1979). 2 Instituto Multidisciplinario de Biología Vegetal, Universi¬ In contrast to the specialization of thehummingbird - dad Nacional de Córdoba, CONICET, Argentina. flower interactions, those involving New World Ex aequo nectar-feedingpasserines are relatively unspecialized

71 Bol. Soc. Argent. Bot. 37 (1-2) 2002

and similar to the interaction between the Old World the introduced white-eye, and also by rats. F. perching birds and their flowers (Stiles, 1981). The reineckeiis visited by flying foxes (Bats,Pteropidae), “dogma” that New World bird-flowers are exploited the starling Aplonis atrifuscus and the pigeon by hoveringbirds while Old World flowers are gener- Columba vitiensis (Cox, 1984). ally visitedby perching birds (van der Pijl, 1961) has In South America at least three cases of a very par- been recently dismissed (Westerkamp, 1990). The ticular bird-flower interactionhasbeenrecently studied. presence of the already mentioned passerine perch¬ In Scrophulariaceae, the genus Calceolaria, which ing birds that visit flowers in the New World and the is nectarless throughout, is mainly pollinated by spe- reported cases of hovering visitors in the Old World cializedoil-collectingbees (Vogel, 1974;Molau, 1988; suggest that neither geographical distribution nor Sérsic, 1994). There are about 50 species ofthe genus, systematic affiliation are direct indication of the kind which lack oil-producing glands (elaiophores). As al- of flower-birdinteractions (Westerkamp. op. cit.). temative to oil-flowers otherpollination strategies are Studies of pollination by birds have focused on present. In many cases Calceolaria species may rely nectar as a reward while alternative reward systems on autogamy orpollinationbypollencollecting-bees. have hardly been noticed. In this paper we describe But at least in one species, C. uniflora, a particular the syndrome features (flower morphology, reward kind of bird pollination with food tissues as reward, properties, position of the pollination unit, flower has evolved (Sérsic & Cocucci,. 1996) (Fig. 1). This color display andcommonvisitors), that deviate from species grows within the low vegetation of the the typical omithophilous syndrome. patagonian steppe and forms perennial cushions of nomore than 10 cmheight. The flowers are markedly Plantfood tissues as reward zygomorphic and two-lipped, the saccate lower lip showing a notorious lap folded to the outside of the Simpson &Neff(1981)reviewed the presence of flower. This thick and sharply bounded lap is white, food tissues that serve as nutritive rewards to differ- and contrasts optically against the yellow and red or ent classes ofpollinators. Beetles, bats or birds con- brownishred spotted lower lip. This juicy appendage sume different floralor extra-floralparts whilepolli- is eaten by the fruit- and seed-eatingbird, Thinocorus nating species of Nymphdea (Nymphaeaceae), rumitivorus, member of the family Thinocoridae, Bactris (Arecaceae) or Freycinetia (Pandanaceae). (Sérsic & Cocucci, 1996). This family doesnot include These authors confirmed that food tissues are also flower-birds of any kind, since they don’t show spe- an alternativerewardthat flowers offer to birds.How- cialized morphological adaptations and they forage ever, whenreviewingplant-birdinteractions Proctor for food on the groundby walking rapidly across the et al. (1996), disregarded the importance of solidre- low vegetation. Calceolariafothergillii, endemic of wards to this kind ofpollinators. the Malvinas Islands, is the only species in the genus that shares the striking floral features of C. uniflora, Individual cases of birdpollination with food tis- suggesting that it could also be similarly bird polli- sues as reward nated(Vogel, 1974; Sérsic & Cocucci, 1996). In Myrtaceae two cases have been described in In the Old World some observations have been tworelatedgenera ofsmall trees (Fig. 2).Acca(Feijoa) reported: Osmoxylon (Araliaceae) fromMalaysia at- sellowiana produces flowers with 4 fleshy sweet pet- tracts birds (pigeons) by means of fruit imitations, als, and numerous stamens. They are visitedby pollen whichconsist on sterile flowersplacedbetweennor- foraging insects and by birds, which feed on petals. mal ones (Faegri & van der Pijl, 1979). This case is known since long (Müller, 1886) and has Freycinetiafunicularis {Pandanaceae) from Asia repeatedly appeared in the literature (Popenoe, 1920; provides fleshy, sugary bracts surrounding the flow- Sick, 1986). (Though,vanderPijl, 1961) dismissed the ,ers. These are eaten particularly by bulbuls presence ofediblepetalsinthis species, Stewart (1986) (Pycnonotidae) which act as pollinators, (Proctor & and Stewart &Craig(1989) showedthatbirds aremore Yeo, 1973). Cox (1983) showed that the bird-polli- important than insects as pollinators òf Acca under natedF. arbórea fromHawaii was originally visited cultureinNew Zealand,USA andJapan. A similar syn- by the endemic, and now almost extinct birds drome has been hypothesizedby Landrum (1986) and Psittirostra psittacea, Loxiodes kona and Corvus Nic Lughadha&Proença(1996) andrecently described tropicus, and in recent years by Zosteropsjapónica, forMyrrhiniumatropurpureum (Roitmanetal.,1997).

72 G. G. Roitman et al.t Flower food tissues as reward for birds

i A B r Q

' \ j . , wm ¿¿a i t KM ii 1 ).5 cm, c ? Sa¿' ¿V D • ?* ÍM mr i * f. j mmA l ,'

mf _ , *-si Fig.l: A-C Calceolaria uniflora. A: cushion of plants with intact flowers; B: one flower with the food tissue partially pecked. C: cushion of plants where almost all flowers show the appendage completely removed. D.Thinocorus rumicivorus (female).

The flowers ofMyrrhinium bear also fleshy petals but reward. Sugar concentration is 14 % in the petals of the reduction in the number of stamens and conse- Myrrhinium (Roitman etal., 1997), 2.14 %in the ap- quently inthe amount ofpollenoffered seems a further pendage ofCalceolaria (Sérsic & Cocucci, 1996) and step towards specialization, because pollenis more ef- 0.23- % and 1.35 %, respectively in the bracts of the ficiently transferred. Fourteen species of fruit- or seed carpellate and staminate inflorescences ofFreycinetia eatingbirds includingMimidae, Tyrannidae, Turdidae, reineckei(Cox, 1983). These concentration values are Thraupidae, Emberizidae, Parulidae, and Icteridae coincident withthose ofgenerally low food-value fruits have been observed removing the sweet petals or nectar offeredby bird-pollinatedplants (Moermond (Roitmanetal., 1997). & Denslow, 1985; Herrera, 1987; Cox, 1983; Dafiii, 1994). Syndrome Position of the pollination unit: In all cases known flowers are not pendulous for this Some of the features already mentioned for ornithophilous category. They are exposed in omithophilous pollination differ or are completely branches and open in an upright position allowing absent in this special category of bird pollination añ access to pollinators from different angles. The with food tissues as reward. These traits could help two-lipped flowers of Calceolaria uniflora make an to recognize a syndrome by identifying conver- exception, since flowers are exposed at ground level gences between unrelated taxa. Following are the allowing the access only from one direction. more salient convergent traits found: Visitors: They usually belong to fruit or seed eat- Reward: There’s no nectar. Instead, fleshy and inS grouPs oí birds. Moreover some species belong sweetparts ofa flower or an inflorescence function as t0 families apparently never reported as flower feed- 73 Bol. Soc. Argent. Bot. 37 (1-2) 2002

A C

150 cm

3 cm D B 1 G

30 cm i E u ***• - ..«r ' • S

1 _5cm i 2 cm Fig. 2: A-B .teca sellowicma. A: Intact flowers. B: flower showing two petals partially removed (arrows). C-E: Myrrhinium atropurpureum. C: aspect of the tree. D: flowering branch. E: flowers. F: Saltator aurantiirostris, arrows show the places where pollen were placed. G: Turdus ruflventris a common visitor to both Acca and Myrrhinium. ingbirds, like Thinocoridae, Turdidae andMirtiidae. ally involves animal learning is floral color change Color: Therewardis self-announcing,unlikenec¬ (Weiss, 1991). In most cases (ca. 220 genera of 74 tar, the presence of which needs to be revealed by families of flowering plants) insects learn to distin¬ coloration of other flower parts (nectar guides). The guish and visit pre-change flowers (where the re¬ foodtissue normallyresembles a fruit witha vividand ward is available), instead of post-change flowers contrasting coloration withinthe flower. Thepresence (rewardless) that only increase the plant attractive¬ of a contrasting bicolored display, like that occurring ness to pollinators at a distance (Weiss, 1991). In both in Myrtaceae and Calceolaria, enhances avian these Myrtaceae the reward is present in the post¬ visits for fruit removal in Prunas serótina and change flowers, while pre-change flowers may in- Phytolacca americana (Willson& Melampy, 1983). crease the attractiveness. These features resemble In Calceolaria uniflora the food tissue maintains those present in omithochorous interactions where its white color during the whole anthesis, simulating color signals may be used to indicate which fruits a juicy fruit. At the site where these plants grow, a are ripe (post-change) and ready for dispersal variety of fleshy omithocorous diaspores are also (Willson & Melampy, 1983). Since part of the peri¬ recognizable at ground level, such as those from anth is removed, the attractiveness of the flower di¬ Berberís empetrifolia, Empetrum rubrum, Ephedra minishes when exploited, thus reducing the prob¬ frustillata and Pernettya mucronata. ability of successive visits. In Myrrhinium and Acca color changes of the Floral construction (architecture): Ornitho- petals are very peculiar. Petals are first dark red philous flowers with food tissues as rewards show (Myrrhinium) or pale pink with a dark red center the bilabiate and the brush type architectures. (Acca) and turn to gray and completely white re¬ Instead, tubular flowers, very widespreadin the nec¬ spectively (Roitman et al., 1997). One trait that usu- tar omithophilous ones, are not represented.

74 G. G. Roitman et at., Flower food tissues as reward for birds

Origin natedgroups. The family Colletidae(Hymenoptera) is considered the most primitive among bees, and Cox (1991) suggested that vertebrate pollination Euryglossinae the most primitive subfamily among and dioecy are ancestral conditions inPandanaceae, them. Members of this subfamily are restricted to a primitive group ofLiliopsida that may have lacked Australian Myrtaceae on which they principally col- nectaries “ab initio'”, while anemophily and entomoph- lect pollen, (Michener,,1965). Australia and South ily are derivedinthe family. America were never in direct contact but were joined Althoughpollination efficiency and effectiveness by Antarctica, though the effectiveness as a faunal of bees and birds may vary greatly4, many cases of bridge was limitedinearly Tertiary to organisms able omithophily have demonstrated that they evolved to tolerate cool temperate climates (Michener, 1979). from bee-pollinated groups, see Gottsberger (1993). There are no Euryglossinae out of Australia and, co- Myrrhinium, Acca and Calceolaria seem to be ex- incidentally, theMyrtaceae arepoorly diversifiedelse- amples ofthiskindoforigin. where, except in South America. In the tropical and The geographic distribution of the oil secreting subtropical regions of Central and South America, Calceolaria species and their oil bees overlap. Myrtaceae species are mainly pollinated by Apidae, About 22 % of the total Calceolaria species have AnthophoridaeandHalictidae(Proença& Gibbs,1994; developed no elaiophores, the proportion of Nic Lughadha & Proença, Í996). According to Nic elaiophoreless species increasing at higher latitudes Lughadha& Proença(1996),thepresence ofnectar in to the North and South (Sérsic, 1994). There are no the flowers of the Myrtaceae is basal, while the nu- collections ofoilbees over 43° S, althoughtherange merous pollen-flower genera of the Myrtoideae lost of Calceolaria is broader. The harshpatagonian cli- their nectary secondarily. mate at these latitudes, with low temperatures and extremely strong winds,may have limited the distri- Concluding remarks bution of the oilcollectingbees, which are normally adapted to more moderate climates. The presence of food tissues as reward for birds The absence of the required bees and the natu- is rare in the Angiosperms and appeared indepen- ral tendency ofsome birds topractice flower preda- dently in only few species of three families of the tion5 probably promoted the origin of this interac- Magnoliopsida and one of the Liliopsida. tion between birds and Calceolaria (Sérsic & Thisparticularpollination strategy evidently has Cocucci, 1996). Althoughmembers ofonly one spe- not evolved from true omithophilous flowers with cies ofbirds have been observed visiting the flow- nectar as reward but probably derived from insect ers of Calceolaria, the possibility that other birds pollinated ancestors.It isnoteworthy that most cases with similar habits also pollinate them is not dis- - mentionedof flowers with food tissues as reward for carded. Seed-eatingbirdslike theEmberizidaemem- birds are philogenetically related to nectarless taxa. bers Melanodera melanodera and M. xantho- Freycinetia is included in the family Pandanaceae gramma and Turdusfalklandii (Turdidae) are also with the anemophilous genus PandanUs and the frequently present in the area and appear as poten- pollen-rewardingbeetlepollinatedSararanga (Cox, tialpollinators. 1990). The closestrelatives of theMyrrhinium-Accd The biogeography and the mainpollinators of the complex havepollen flowers exploitedby bees (Ñic two omithophilous Myrtaceae species may give a Lughadha & Proença, 1996), andfinally,Calceolaria possible explanationoftheir evolutionfrombeepolli- uniflora is included in a mainly oil-rewarding bee- pollinated genus (Sérsic, 1994). Only few morpho¬ 4For example, bumble bees deposited 10 times more pollen logical changes were necessary in these flowers or per visit than hummingbirds in Delphinium neisonii flowers, but within a population hummingbird visitation rates are 10 inflorescences to produce profound changes in their times higher than those ofbumble bees Waser & Price (1990). pollination strategies. Although thepollinationunits . 5ln fact, Musisaxicola alpina (Tyrannidae) was observed here involvedare well adapted for visitationbybirds, eating corollas of the oil-bearing and normally bee- there are no evident adaptations of the birds to the pollinated Calceolaria brunellifolia in Mendoza (Argenti¬ plants and they feed opportunistically on food tissues na); also many passerine bird’s were observed taking nectar as well as eating the corollas of Anarthrophyllum as wellas ona variety offruits. Simpson&Neff(1981) desideratum (Papilionaceae) which occurs together with concluded that selection favored the elaboration of a C. uniflora (Sérsic, unpübl.). different reward either to capture a segment of the

75 Bol. Soc. Argent. Bot. 37 (1-2) 2002

pollinator community not used by other plants or to COX, P. A. 1983. Extinction of the Hawaiian avifauna re¬ sulted in a change of pollinators for the ieie, Freycinetia achieve greater pollinator constancy. These changes arbórea. Oikos 41: 195-199. usually promote a one-to-one relationship and / or a and ornithophily in reward. However, in both Acca and COX, P. A. 1984. Chiropterophily more expensive Freycinetia (Pandanaceae) in Samoa. Plant Syst. Evol. Myrrhinium, their relationship to birds is still diffuse, 144: 277-290. them, the sincemany bird species visit and reward qual¬ COX, P. A. 1990. Pollination and the evolution of breeding sys¬ ity has not been increased, in comparison to that of tems in Pandanaceae. Ann. Missouri Bot. Gard. 77: 816-840. nectar or fruits. Nevertheless, the production of “fruit- COX, P. A. 1991. Abiotic pollination: an evolutionary es¬ like”petals enables theseplants to attract a new kindof cape for animal- pollinated angiosperms. Phil. Trans. pollinators (birds) different fromthoseprevalentinmost Royal Soc. London. Series B 333: 217-224. Myrtaceae and Calceolaria (bees). The Acca and DAFNI, A. 1994. Pollination ecology: A practical approach. Myrrhinium plant-bird interaction seems to be an IRL Press, Oxford. unspecialized one and it wouldbe the outcome of dif¬ FAEGRI, K. & L. van der PIJL. 1979. The principles of fuse coevolution(Janzen, 1980, Jordano, 1987). These pollination ecology. Pergamon Press, Oxford. characteristics contrast with the highly coevolved FEINSINGER, P. 1991. Interacciones entre plantas y colibríes oligotropic omithophilous systems frequently found en selvas tropicales. Bol. Acad. Nac. Ciencias. Cordoba. 59: 29- 54. in the Neotropics, but are similar to the paleotropical allotropicFreycinetiareineckie. Thelatter ispollinated GOTTSBERGER, G, 1993. Floral ecology: F. Special Top¬ ics. I. Progr. Bot. 54: 461-504. Springer Verlag Berlin, by bats and birds in Samoa in which the reward are Heidelberg. fleshybracts,(Cox, 1990). HERRERA, C. M. 1987. Vertebrate-dispersed plants of the The origin and explosive diversification of flower¬ Iberian Peninsula: a study of fruits characteristics. Ecol. ing plants during Cretaceous is often attributed to a Monog. 57: 305-331. simultaneous evolutionary radiation of insects, which JANZEN, D. H. 1980. When is it coevolution?. Evolution 34: servedas criticalpollenvectors. Vertebrates are thought 611-612. to have played an insubstantial role in early evolution JORDANO, P. Í 987. Patterns of mutualistic interactions of angiosperms because the main groups, which are in pollination and seed dispersal: connectance, depen- important pollinators of extant plants taxa (birds and dence, asymmetries, and coevolution. Amer. Nat. 129: 657-677. bats), originated no earlier than the Eocene, (Kress & Stone, 1993). Insect pollination was probably the pre¬ KRESS, W. J. & D. E. STONE. 1993. Morphology and floral biology of Phenakospermum (Strelitziaceae), an arbores¬ not cursor of hummingbird pollination, only because cent herb of the Neotropics. Biotropica 25: 290-300. insects were first on scene but also because intermedi¬ LANDRUM, L.R. 1986. Monograph 45. Campomenesia, ate processes are visible nowadays (Stiles, 1981). Pimienta, Blepharacolyx, Legrandia,- Acca, Myrrhinium and Luma (Myrtaceae). Flora Neotropica, The New York Botanical Garden, New York. ACKNOWLEDGMENTS MICHENER, C. D. 1965. A classification of the bees of the Australian and South Pacific regions. Bull. Am. Nat. Hist. 130: 1-362. We are gratefultoD.Medan and J. J. Valla for con¬ MICHENER, C. D.- 1979. Biogeography of bees: Ann. Mis¬ structive criticism to an earlier draft. To L. Galetto for souri Bot. Gard. 66: 277-347. on Partial financial support comments the manuscript. MOERMOND T. C. & J. S. DENSLOW. 1985. Neotropical was provided by the National Research Council avian frugivores: patterns of behavior, morphology and (CONICET) to whichANS and AAC aremembers. nutrition, with consequences for fruit selection. In: P. A. BUCKLEY, M. S. FOSTER, E. S. MORTON, R. S. RIDGELY & F. G. BUCKLEY (eds.). Neotropical Orni¬ thology: pp. 865-897. Ornithological Monographs 36. BIBLIOGRAPHY American Ornithologists’ Union, Washington.- MOLAU, U. 1988. Scrophulariaceae. Part i. Calceolarieae. ARMSTRONG, J. A. 1979. Biotic pollination mechanisms Bòt. Gard. Bronx, New York. in the Australian flora - a review. New Zeal. J. Bot. 17: MÜLLER, F. 1886. Feijoa, ein Baum der Võgelm Seiner 467-508. Blumenblãtter ais Lockspeise bietet. Kosmos 1: 93-98. BRUNEAU, A. 1997. Evolution and homology of bird polli¬ NIC LUGHADHA, N. & C. E. B. PROENÇA. 1996. A sur¬ nation syndromes in Erythrina (Leguminosae). Amer. J. vey of the reproductive biology of Myrtoideae. Ann. Bot. 84: 54-71. Missouri Bot. Gard. 83: 480-503. G. G. Roitman et a!., Flower food tissues as reward for birds

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