pollination mechanisms in four sympatric southern ...

Lindleyana 14(1): 47-56. 1999.

POLLINATION MECHANISMS IN FOUR SYMPATRIC SOUTHERN BRAZILIAN EPIDENDROIDEAE ORCHIDS 1 RüDRIGO BUSTOS S!NGER 2 ·3 AND ANDREA

A.

COCUCCI 4

'Departamento de Pós-graduação Botânica, Universidade Federal do Paraná, Curitiba, Paraná, Brazil "Instituto Multidisciplinário de Biologia Vegeta, Córdoba, Argentina

ABSTRACT: The pollination process is reported for the first time in four epidendroid orchids which occur sympatrically in Curitiba, Paraná, southern Brazil. Capanemia thereziae (Maxillarieae: Oncidiinae) is pollinated by Polybia fastidiosuscula (Vespidae) wasps which drink nectar in a shallow nectary on the surface of the lip. Maxillaria picta (Maxillarieae: Maxillariinae) is pollinated by Trigona spinipes (Apidae, Meliponinae) workers which are deceived, as flowers offer no reward. Pleurothallis luteola (Epidendreae: Pleurothallidiinae) is pollinated by Megasellia sp. flies (Phoridae) which apparently obtain nectar on the surface of the lip. A male Tetrapedia diversipes (Anthophoriidae: Tetrapediini) bee was caught at flowers of Oncidium paranaense (Maxillarieae: Oncidiinae). lt removed pollinaria and gathered oi! from the elaiophores on the lateral lobes of the lip.

MosT EXISTING information about orchid pollination in South and Central America was reviewed by Dressler (1981, 1993), van der Pijl and Dodson ( 1966), and Roubik and Ackerman (1987). In Brazil, the only study involving a whole orchid flora was published by Braga ( 1977), who studied and described in detail the pollination process of a number of orchid species in central Amazonia. During a two-year study of

the orchid flora of Curitiba, Paraná, southem Brazil, we recorded and illustrated the pollination process in many species, and part of those results are presented here. The aim of the present paper is to present information conceming part of a flora for which no pollination record has been published.

MATERIALS AND METHODS Field studies were done in a 2-ha remnant of

' A substantial part of this work was presented by the first author as part of his M.Sc. thesis in botany at the Universidade Federal do Paraná in Curitiba, Paraná State, Brazil. We want to thank Prof. Alain François for English improvement, Prof. Yedo Alquini (Pós-graduação em Botânica); our colleagues Cleber lbrahim Salimon, Vinicius Bittrich, and Carina Kozera for assistance and help in many ways; Prof. Albino Sakakibara (UFPR, Dept. Entomologia) for photographing the pinned insects; Profs. Padre Jesus Santiago Moure, Danuncia Urban, M. Cristina de Almeida (UFPR, Dept. of Entomology), and Prof. Ediberto Giannotti (UNESP) for insect identification; and Prof. Marlies Sazima (IB, UNICAMP) for suggestions and comments on the manuscript. The first author wants to thank Dr. R. L. Dressler who helped with patience (and papers) to resolve our morphological doubts. The comments and suggestions of Prof. Norris Williams and an anonymous reviewer are greatly acknowledged. This work was made possible by a CAPES (Coordenação de Aperfeiçoamento do Pessoal de Ensino de Nível Superior) grant, which is greatly acknowledged. The second author is grateful to the Departamento de PósGraduação em Botânica da Universidade Federal do Paraná, Curitiba (UFPR) and to its then director (Prof. Dr. Yedo Alquini) for making possible a three-month teaching and study leave in Curitiba. ' Author for correspondence: Departamento Botânica-IB, Universidade Estadual de Campinas, UNICAMP, Caixa Postal 6109, C.E.P. 13083-970, Campinas, São Paulo, Brazil.

an

Araucaria stand, at the campus of the Univ-

ersidade Federal do Paraná, Curitiba, Paraná State, southern Brazil (25°25'S, 49°17'W, elevation 900 m). Annual rainfall is about 1450 mm, and the annual average temperature is about 16.5 C (Maack, 1981).

Araucaria angustifolia (Bert)

Kuntze (Araucariaceae) is the dominant tree species in the area. The original vegetation before clearing was a transition between Araucaria forest and natural grasslands (Maack, 1981). Field visits were undertaken to observe and record the pollination processes and to capture pollinators for later identification. During initial visits fresh orchid flowers were fixed in 70% alcohol and later drawn in the laboratory using a binocular stereomicroscope with camera lucida attachment. Plant vouchers are deposited at the herbarium of the Universidade Federal do Paraná (UPCB). Osmophores (scent-producing glands) were lo47

SINGER AND COCUCCI-POLLINATION MECHANISMS IN BRAZILIAN ORCHIDS

cated by submerging fresh fiowers of the four species in a 1: 10,000 neutral red dye in tap water (Vogel, 1963). Nectar was located with little strips of glucose-reactive paper, as suggested by Kearns and Inouye (1993). Oils were identified by contact with Sudan III dye, which is specific for lipids and gives a reddish coloration to oils if present (Forster, 1949). The pollination process in Capanemia thereziae Barb.Rodr. (Maxillarieae: Oncidiinae) was studied in six visits from 15 August to 5 September 1995 and in an additional visit on 5 September 1996, for a total of 20 hr of observation. The observation period extended from 9:00 to 13:00. Observations were made on seven plants which produced up to 50 fiowers in 1995. In 1996, fiower number was considerably lower (about 30 fiowers). The pollination process in Maxillaria picta Hook. (Maxillarieae: Maxillariinae) was studied in eight visits, three of which were between 1629 July 1995 and tive between 3-8 August 1996, for a total of 30 hr of observation. Three additional field visits were undertaken from 9-11 August 1996 only to check the fiowers without further observations. The observation period extended from 9:00 to 14:00, following a plant (the last remaining in the study area) which produced 16 fiowers in 1995 and 21 in 1996. The pollination process in Oncidium paranaense Kraenzl. (Maxillarieae: Oncidiinae) was studied over 16 field visits between 25 November and 14 December 1995, for a total of 48 hr. Observations were made on two plants with one infiorescence each. Both produced up to 120 fiowers during the period. The observation period extended from 10:00 to 13:00. The pollination process in Pleurothallis luteola Lindl. (Epidendreae: Pleurothallidiinae) was recorded in 12 field visits from 22 February to 26 March 1996, for a total of 42 hr of observation. The observation period extended from 9:00 to 18: 30. Observations were made on two plants, which produced about 40 fiowers during the period. Pollinators were captured at the fiowers, photographed with a 35 mm Zeiss stereomicroscope, and sent to specialists for identification. In all cases, field notes were taken conceming the pollinator's behavior at the fiowers. To illustrate the morphological interaction between pollinators and fiower parts, longitudinal sections of fiowers

and fresh insects with pollinaria were manipulated under the stereomicroscope, and the resulting interactions were drawn. Insect vouchers are deposited at the entomological collection at the University of São Paulo (USP). Throughout this text, the systematic concepts of Dressler (1993) are followed.

RESULTS Capanemia thereziae is a little epiphyte which usually grows on Campomanesia sp. (Myrtaceae) and Vernonia sp. (Compositae) trees, mostly in open areas near bogs. Each plant produces 1-3 lateral racemes with 2-4 fiowers each. The fiowers (Fig. lA) are resupinate, greenish yellow, and approximately 6 mm in diameter. The dorsal sepal is elliptic-lanceolate, acute, about 3 mm long and 2 mm wide. Lateral sepals are falcate, acute, somewhat asymmetric, about 5 mm long and 2 mm wide. Lateral petals are elliptic-lanceolate, acute, about 4 mm long and 2 mm wide. The lip is entire, acute, about 5 mm long and 3 mm wide. The column has two lateral wings (Fig. IB). The anther is incumbent and bears a pollinarium consisting of two yolk-yellow, waxy pollinia, caudicles, a laminar stipe, and a dark, elliptic viscidium (Fig. 1C). The stigma is entire and cone ave. The fiowers lack any perceptible fragrance. There are two parallel calli (Fig. IA) at the lip base, where nectar is secreted and offered in a shallow position. Flowers may keep their fresh appearance for about a week. Plants were found in bud in late July, in fiower in early and mid-August, in fruit in mid- and late August, and dehiscence was observed in late December. Pollinator acti vity was noted between 11 :00 and 13:00. Pollinators were females wasps of Polybia fastidiosuscula Saussure 1854 (Vespidae). They visited the fiowers at intervals of 1-38 minutes. The wasps did not directly alight on the fiowers but hovered in front of them for some seconds. Since infiorescences are pendulous and in some instances lie on the surface of the tree, wasps can walk on the tree to visit the fiowers. Otherwise wasps use the whole infiorescence as a landing platform, since fiowers are not big enough for them to enter completely. Insects visit about 5-7 fiowers in a single visit, leaving the infiorescences after 15-30 seconds. Wasps drink the nectar stored at the base of the lip (Fig. 3A) 48


to the lip, which tips down and allows access (Fig. 4A). The lip recovers its original position when the insect is completely inside the perianth (Fig. 4B). The insect stays for 7-20 seconds in the fiower, apparently searching for nectar. When it backs out to leave the fiower, the floral exit is narrow, and it must force its way by pressing against the column with its body and thereby removing the pollinarium, with the viscidium fixed on the bee's scutellum (Fig. 4C; Fig. 7B). If the bee leaves the fiower in a straight line, the whole viscidium embraces the scutellum, but we observed that in some instances bees leave the fiowers somewhat laterally, and part of the viscidium remains free from the bee's scutellum. When the pollinarium is removed, the anther cap falls almost immediately (Fig. 4D). The bee stays for a few seconds on the edge of the lip and finally fiies away. We had the impression that the bees became somewhat drowsy, perhaps due to the fiower's strong fragrance. We did not observe pollinaria deposition. However, from a morphological point of view, the process may be similar to that of pollinarium removal. A pollinarium carried by a bee may be retained by the stigma when the insect exits the fiower. Oncidium paranaense is an epiphyte with bifoliate pseudobulbs and lateral panicle commonly found in open areas. The fiowers (Fig. IG) are yellow with brown spots and about 7 mm in diameter. Sepals are elliptic, acute, and about 3 mm long and 2 mm wide, the lateral ones somewhat asymmetric. Lateral petals are obtuse with approximately rectangular margins, about 3 mm long and 2 mm wide. The lip is 3-lobed, about 5 mm long and 4 mm wide. The colurnn has two lateral wings and a tabula infrastigmatica (Dressler, 1981) at its base (Fig. IH). The anther is incumbent and bears a pollinarium with two clavate, yolk-yellow pollinia, caudicles, a spathulate stipe, and a dark, elliptic viscidium (Fig. li). The stigma is entire and concave. Fragrance is produced by the middle portion of the lip, which is very thick and papillose. Each lateral lobe of the lip bears an epidermal elaiophore, the oil held under a thick cuticle (Fig. 2). The fiowers keep their fresh appearance for about 15 days. Plants were in bud in mid-November, in fiower from late November until late December, and in fruit from early to mid-December. Dehiscence occurred in early March.

and when doing so remove the pollinarium, which adheres to the clipeum (Fig. 3B), just below the antennae. The anther cap does not fali after pollinarium removal. A single wasp can carry several pollinaria (Fig. 7A), which may disturb those insects in some way since they were observed in some instances trying to clean the pollinaria from the clipeus with their forelimbs. When a wasp carrying pollinaria visits another fiower and drinks nectar (Fig. 3C), it leaves the pollinia (rarely a whole pollinarium), which are easily retained by the stigma (Fig. 3D). Maxillaria picta is an epiphyte with bifoliate, quadrangular pseudobulbs. The fiowers are solitary and lateral. A single plant may produce many fiowers. Flowers (Fig. ID) are resupinate, yellow with purple spots, and about 35 mm long. The dorsal sepal is lanceolate, acute, about 30 mm long and 1O mm wide. Lateral sepals are lanceolate, acute, about 30 mm long and 7 mm wide. Lateral petals are also lanceolate and acute, about 30 mm long and 4 mm wide. The lip is hinged at the base of the column, 3-lobed, obtuse, and about 18 mm long and 10 mm wide. The colurnn has no lateral appendages (Fig. IE). The anther is incumbent and holds a pollinarium which consists of four yolk-yellow, waxy pollinia, caudicles, and a broad, saddle-like viscidium (Fig. IF). The stigma is entire and concave. The fiowers have a strong honey-like fragrance which is produced by the inner surfaces of the entire perianth. Flowers lack nectar or any other reward. Flowers may keep their fresh appearance for about 15 days. Plants were found in bud in early July and fiowering from then until August. Some fiowers began to develop fruits in late June 1995, aborting a few days later. No fruits were observed in 1996. Pollinator activity was observed between 10:00 and 14:00. The observed pollinators were workers of Trigona spinipes Fabricius 1793 (Apidae: Meliponinae). In the observations made in 1995 we captured bees with pollinaria, which were fiying near the plant, but insect behavior at the fiowers was recorded only in 1996. During the observation period, consecutive visits to fiowers were observed at intervals of 10-58 minutes. It is noteworthy that insects were interested in the fiowers for only a few days, and additional field visits indicated that no more pollinaria were removed five days after the fiowers opened. The bee alights on the surface of the lateral sepals and then walks 49

SINGER ANO COCUCCI-POLLINATION MECHANISMS IN BRAZILIAN ORCHIDS

L__j

1mm

c

L_____j

1mm

L___j

1mm

D

L___j

10mm

F l__j

1mm

l..__j

L.___j

1mm

1mm

~

w

K

L L_j

1mm

J l___j

2mm

50

L_____j

1mm


Fig. 2.

Oncidiwn paranaense. Gross anatomical structure of an elaiophore (c: cuticle; o: oi!; e: epidermal secretory layer). Bar= I JLITI.

In the entire observation period, only one visitor was recorded and caught at fl.owers (at approximately 11 :30). lt was a male Tetrapedia diversipes (Anthophoridae: Tetrapedini; Fig. 7C) which visited a few fl.owers for about 30 seconds before being captured. The bee collected oil in the elaiophores, hovering in front of the fl.owers while passing the oil from its forelimbs to the scopae, and removed four pollinaria which were fixed on the clipeum (Fig. 7C). Pleurothallis luteola is a pseudobulbless epiphyte with long, petiolate, elliptic-lanceolate, and pendulous leaves. These plants are common in Curitiba, particularly in shaded, hurnid areas. Infl.orescences are terminal, epiphyllous, and condensed, 1-3 fl.owers being gradually produced in a short pedicel. The fl.owers (Fig. lJ) are resupinate, more or less tubular, yellow with dark purple spots on the surface of the lip, and about 12 mm long. The dorsal sepal is elliptic, obtuse, about 7

mm long and 3 mm wide. Lateral sepals are connate, free only at the apex, each one 4 mm long and 1 mm wide. Lateral petals are spathulate, acute, somewhat asymmetric, and about 3 mm long and 1 mm wide. The lip is hinged at the base, auriculate, and about 4 mm long and 2 mm wide. The colurnn has two lateral wings and is notably omamented around the anther (Fig. lK). The anther is incumbent, with a pollinarium consisting of two yellow, clavate pollinia prolonged into hyaline caudicles (Fig. lL). The stigma is entire and concave, the rostellar fl.ap being also markedly concave. Flowers have a very slight, sweet fragrance which is produced in a thickened area at the inner edge of the dorsal sepal. The surface of the lip is papillose, always wet in fresh fl.owers, and may be a nectary. Glucose-reactive strips did not react on the surface of the lip, but this could be due to the very small quantity or the density of the liquid.

Fig. I. Flower features. A-C. Capanemia thereziae. A. Flower, front view. B. Column, lateral view. C. Pollinarium. D-F. Maxillaria picta. D. Flower. E. Column, ventral view. F. Pollinarium. G-1. Oncidium paranaense. G. Flower, lateral view. H. Column, front view. I. Pollinarium. J-L. Pleurotha/lis luteola. J. Flower, lateral view. K. Column, ventral view. L. Pollinarium (e: elaiophores; t: tabula infrastigmatica; ca: calli).

51


Fig. 5. Megasellia sp. (Phoridae) fly at fiowers of Pleurothal/is luteola. Bar= I mm.

may function as nectar guides. When a fly passes under the column, the lip tips down, recovering its original position when the insect has fully entered (Fig. 6B, F). The fty repeatedly examines the surface of the lip and may stay at the flower for about 15-120 seconds. The floral exit is somewhat narrow, since the lip bends down enough only when the insect is at its edge. Therefore, when the fly attempts to back out, it must force its way through the narrow opening for about 115 seconds, pressing its dorsal thorax against the column (Fig. 6C). lts scutellum is coated with rostellar cement at the rostellar flap and then touches the caudicles which firmly stick to it. As a result the whole pollinarium (including the anther cap) is removed (Fig 6D). The anther cap usually remains, covering the pollinarium for 20-60 minutes or more. However, the anther cap may fall

Fig. 3. Pollination mechanism in Capanemia thereziae by Polybia fastidiosuscula wasps (Vespidae). A. The wasp licks nectar in a shallow nectary at the base of the lip. B. The pollinarium adheres just below the antennae, and the wasp leaves the fiower. C. A wasp carrying a pollinarium visits the flower and licks nectar, touching the stigma with the pollinia. D. The pollinia are left in the concave stigma, and the wasp leaves the flower.

Plants were found flowering from late February until late March, when fruits were recorded. Dehiscence was observed in September-October. Pollinator activity was recorded between 11:00 and 16:00. Pollinators were flies of Megasellia (Phoridae; Fig. 5, 6, 7D). Consecutive visits to ftowers were observed at intervals of 1-40 minutes. The fties walk or fty to the ftower and then walk from the lateral sepals toward the lip (Fig. 6A), apparently following the dark spots which

Fig. 4. Pollinarium remova! in Maxillaria picta by Trigmw spinipes (Apidae: Meliponinae) worker. A. After landing on the dorsal sepal, the bee walks toward the lip, which tips down. B. The bee totally enters the fiower, and the lip recovers its original position. C. When leaving the fiower, the bee removes the pollinarium, so that the viscidium adheres to the scutellum. D. Immediately after pollinarium remova! the anther cap falls.

52


B

~

~ F

Fig. 6. Pollination of Pleurothallis luteola by Megasellia sp. (Phoridae) flies. A. The fly walks toward the lip, probing its surface. In response to the fly's weight the lip tips down. B. When the fly completely enters the flower, it passes the equilibrium point, and the lip recovers its original position. C. When leaving the flower, the fly presses with the scutellum against the rostellar flap. The scutellum is coated with rostellar glue which fixes the caudicles. D. The whole pollinarium is removed. E. A fly carrying a pollinarium visits a flower, and the lip tips down because of the fly's weight. F. The fly enters the flower, and the lip recovers its original position. When the fly leaves the flower, pollinia are retained in the concave stigma. G. The pollinarium is deposited on the stigma, and the fly leaves the flower.

off, in part by desiccation but also because the insects repeatedly attempt to clean their thorax with their legs and wings. When a fly carrying a pollinarium visits another flower (Fig. 6E-F) and attempts to back out, morphological interactions occur in a similar manner, this time the pollinarium being caught by the stigma (Fig. 6G). When a fly carries a pollinarium still covered by the anther cap, the latter is deposited instead of the pollinarium.

local orchid flora of Curitiba there are at least three additional species in Oncidiinae bearing elaiophores: Oncidium loefgrenii Cogn., O. unicome Lindl., and Sigmatostalix radicans Rchb.f., the latter having elaiophores similar to those of O. paranaense (pers. observ.). This is the first pollination report for Capanemia. Wasp pollination is a well documented phenomenon in a number of Old World orchids (Adams and Lawson, 1993; van der Pijl and Dodson, 1966), but records for the Americas are scarce. Van der Pijl and Dodson (1966) reported wasp pollination in species of Brassia (Oncidiinae) and Encyclia (Laeliinae) by Campsomeris (Scoliidae) wasps. Chase (1986) and Dressler (1981) recorded pollination in species of Leochilus (Oncidiinae) by social wasps (Vespidae) which, as Polybia wasps do in Capanemia thereziae, drink nectar from shallow nectaries on the lip. Capanemia comprises about 14 species (Dressler, 1993), some of which may be pollinated by little bees. In some instances we have observed halictid bees alighting and visiting Capanemia australis Barb.Rodr. in Curitiba (pers. observ.), but we still

DISCUSSION All the studied orchids have floral features which are common or well known in the genera and suprageneric ranks to which they belong (Dressler, 1981, 1993). The elaiophores in Oncidium paranaense are interesting because they have an expanding cuticle holding the oil secreted by the epidermis (Fig. 2). This is more similar to the elaiophores found in Malpighiaceae than to the trichomed or epidermal elaiophores (in which the oils are directly secreted from the surface), usually found in orchids of the subtribes Oncidiinae and Omithocephaliinae (Vogel, 1974). In the

53


o

Fig. 7. Pinned insects carrying pollinaria. A. Polybiafastidiosuscula (Vespidae) carrying severa! pollinaria of Capanemia thereziae. B. Trigona spinipes (Apidae: Meliponinae) worker with a pollinarium of Maxillaria picta attached to its scutellum. C. Male Tetrapedia diversipes (Antophoridae: Tetrapedini) with four pollinaria of Oncidium paranaense attached to its clipeus. D. Megasellia sp. (Phoridae) fly with a pollinarium of Pleurothallis /uteola fixed on its scutellum. Bars= 1 mm.

lack evidence demonstrating that these are pollinators. Capanemia australis and Capanemia superfiua Barb.Rodr. (native to Minas Gerais State and absent in Curitiba) have rninute, fragrant, white, yellow-spotted, nectarless flowers which differ considerably from the greenish, scentless, nectar-bearing flowers of C. thereziae. The flower features of C. thereziae agree with the characteristics of wasp-pollinated flowers according to van der Pijl and Dodson (1966). This is the first report on the pollination of Maxillaria picta_ Van der Pijl and Dodson (1966) recorded six pollination reports for Maxillaria, two of which involve stingless Trigona bees. Other pollen vectors such as other stingless bee species, bumblebees, euglossine bees, and even hummingbirds were recorded by these authors_ Although van der Pijl and Dodson ( 1966) discussed aspects of the behavior of Trigona at flowers, they did not mention the mechanism by which the pol-

linarium is removed and deposited_ Trigonas have been registered as pollinators in species of Schomburgkia (Laeliinae) and Xylobium (Lycastinae; van der Pijl and Dodson, 1966) and for a number of Australian species of Caladenia, Cymbidium, and Dendrobium (Adams and Lawson, 1993). Visits to Trigonidium obtusum Lindl. (Maxillariinae) flowers by males Trigona droryana ( = Plebeia droryana) have been considered a case of pseudocopulation by van der Pijl and Dodson (1966). This is actually a rnisinterpretation of the work of Kerr and López (1963), who stressed that these bees were not pollinators since they were not big enough to dislodge the pollinanum. Braga (1977) recorded the pollination biology of Maxillaria pendens Pabst by wasps of Stelopolybia cf pallipes (Vespidae)_ They attempt to collect wax on a callosity of the lip. When leaving the flower the pollinarium is fixed between the 54


matica with their mandibles. Such a behavior, if confirmed, would be similar to that performed by Centris bees, which pollinate Malpighiaceae. While taking oils from the elaiophores with their forelimbs, the bees use their mandibles to grasp constrictions at the base of the petals (Vogel, 1974, 1990). Although there is a consensus that most Pleurothallis (if not all) are fly-pollinated (Christensen, 1994; Dressler, 1981, 1993; van der Pijl and Dodson, 1966), there are only a few published reports for a genus that may have as many as 1,120 species (Dressler, 1993). Four reports involve flies of the genera Lacodrosophila, Lycoria, and Drosophila (van der Pijl and Dodson, 1966). In P. monocardia flies of the genus Lycoria pollinate while drinking nectar collected around the base of the lip, the pollinaria being attached to the legs. More recently, Chase (1985) described the pollination of Pleurothallis endotrachys by Drosophila immigrans. The pollination mechanism detailed by Chase ( 1985) is essentially the same we observed in P. luteola. Chase ( 1985) did not find nectar or any other reward. In the case we studied, even when glucose-reactive paper failed in demonstrating the presence of nectar, we suppose the liquid on the surface of the lip is nectar or at least is exploited by the fties as if it were so. Some Pleurothallis species have nectaries, and some do not (Christensen, 1994; Dressler, 1981). Only two of the six Pleurothallis species found in Curitiba may have nectaries: probably Pleurothallis luteola (for which more information is needed) and Pleurothallis recurva Lindl. The latter species has ephemeral flowers (fresh in appearance 2-3 days) with nectar on the surface of the lip. In this case, the liquid reacts positively with glucose-reactive paper. Retention of the anther cap, which was observed in the pollination mechanism of P. luteola, can increase the chance of cross-pollination since fties are quite passive and return to the same flowers a few times before leaving. Few reports on anther cap retention exist. Catling and Catling (1991) reported anther cap retention for 8-40 minutes in Tipularia discolor, which is pollinated by moths and unrelated to Pleurothallis. They recorded gradual changes in the anther cap, which opens to release the pollinarium. We did not record such changes in P. luteola, and we suppose

antennae or on the eyes. Braga (1977) noticed that the weight of the pollinarium may disturb the insects, since wasps leave the flowers flying in a clumsy way, sometimes colliding with obstacles in the surrounding vegetation. According to Braga, wasps with a pollinarium on an eye cannot fty and may be easily predated by other animais. The observations in Oncidium paranaense were very fragmentary but, to our knowledge, this is the first report of a bee actively collecting oil on ftowers of Oncidium. Former reports (van der Pijl and Dodson, 1966) involved in most cases bees o f the genera Centris, Xylocopa, and Bambus deceived by "food-fraud" flowers, and in others male bees attacking the ftowers which are mistaken as enemies ("pseudoantagonism"). By the time these reports were made, it was accepted that many Oncidium flowers were mimics of malpighiaceous flowers which offered nectar as a reward (van der Pijl and Dodson, 1966). In fact, the resemblance to malpighiaceous ftowers by many oncidiums may not be casual. However, most American malphigiaceous ftowers offer oils as a reward (exactly as many orchids in Oncidiinae and Omithocephaliinae do). Females of Anthophoridae bees of the genera Centris, Paratetrapedia, and others (Vogel, 1974, 1990) gather the oils (and pollen) for nurturing their larvae. An intriguing fact about the bee captured at O. paranaense ftowers is that it is a male. There is some evidence that male bees of the genera Tapinotaspis and Tetrapedia collect oils in way similar to that of females in ftowers of Nierembergia (Solanaceae) and Angelonia (Scrophulariaceae) (Cocucci, 1991; Vogel and Machado, 1991). What exactly the male bees do with the oils remains a mystery and, for now, a matter of speculation. Schlindwein (1995) captured a female of Terrapedia rugulosa carrying pollinaria which morphologically fit an unidentified Oncidium species and hypothesized that the orchid may be an oil resource for the bee. In the context of all the information aforementioned, further observations may confirm that O. paranaense is pollinated by Tetrapedia diversipes bees, males and females alike. A morphological feature in agreement with pollination by oil-collecting bees is the presence of a tabula infrastigmatica (Fig. IH) at the base of the column. Dressler (1981) suggested that bees may stabilize themselves in the ftowers while extracting the oils by holding the tabula infrastig55


- - . !986. Two new species in the genus Leochilus (Orchidaceae). Syst. Bot. 11: 242-246. Christensen, D. E. 1994. Fly pollination in the Orchidaceae. Pages 417-454 in J. Arditti (ed.), Orchid Biology: Reviews and Perspectives, VIII. John Wiley & Sons Inc., New York. Cocucci, A. A. 1991. Pollination biology of Nierembergia (Solanaceae). Plant Syst. Evol. 174: 17-35. Dressler, R. L. 1981. The Orchids: Natural History and Classification. Harvard University Press, Cambridge. - - . !993. Phylogeny and Classification of the Orchid Family. Dioscorides Press, Portland, Oregon. Endress, P. K. 1994. Diversity and Evolutionary Biology of Tropical Flowers. Cambridge University Press, Cambridge. Forster, A. S. 1949. Practical Plant Anatomy. Van Nostrand, New York. Kearns, C. and W. Inouye. 1993. Techniques for Pollination Biologists. University Press of Colorado, Niwot. Kerr, W. E. and C. R. López. 1963. Biologia da reprodução de Trigona (Plebeia) droryana F. Smith. Rev. Bras. Biol. 22: 335-341. Maack, R. 1981. Geografia Física do Estado do Paraná. 2nd ed. J. Olympio-Secret. da Cultura do Estado do Paraná, Rio de Janeiro. Pijl, L. van der and C. H. Dodson. 1966. Orchid Flowers: Their Pollination and Evolution. University of Miami Press, Coral Gables. Roubik, D. W. and J. D. Ackerman. 1987. Long-term ecology of euglossine orchid-bees in Panama. Oecologia 73: 321333. Schlindwein, C. 1995. Wildbienen und ihre Trachtpflanzen in einer sudbrasilianischen Buschlandschaft: Fallstudie Guaritas, Bestiiubung bei Kakteen und Loasaceen. Verlag Ulrich E. Grauer, Stuttgart. Vogel, S. 1963. Duftdrüsen im Dienste der Bestiiubung: Über Bau und Funktion der Osmophoren. Abh. Akad. Wiss. Lit. Mainz. Math. Naturwiss Kl. 10: 598-763. - - . 1974. Olblumen und olsammende Bienen. Abh. Akad. Wiss. Lit. Mainz. Math. Naturwiss Kl. 7: 283-547. - - . !990. History of Malpighiaceae in the light of pollination ecology. Mem. New York Bot. Gard. 55: 130-142. - - and I. C. Machado. 1991. Pollination of four sympatric species of Angelonia (Scrophulariaceae) by oil-collecting bees in NE Brazil. Plant Syst. Evol. 178: 153-178.

that the anther cap falls by a combination of dehydration of both anther cap and pollinia with the action of the flies trying to remove the pollinarium from the scutellum. Catling and Catling (1991) observed that a Tipularia discolor pollinarium covered by the anther cap does not adhere to the stigma when contacting it. In contrast, we observed that a fly carrying a pollinarium with its anther cap may eventually deposit the anther cap instead of the pollinarium. This is the first report involving Phoridae flies in Pleurothallis pollination. Flies of the genus Megasellia have been suggested as "probable pollinators" of the Australian Rhizanthella gardneri (Adams and Lawson, 1993; Christensen, 1994). We have made isolated observations of the same flies which pollinate P. luteola visiting cultivated plants of Pleurothallis pectinata Lindl. in Curitiba. Pleurothallis pectinata does not belong to the local orchid flora but has floral features similar to those of P. luteola. Megasellia flies may perform pollination at least sometimes, since fruits are frequently produced. LITERA TURE CITED Adams, P. B. and S. D. Lawson. 1993. Pollination in Australian orchids: a critica! assessment of the literature 18821992. Austral. J. Bot. 41: 553-75. Braga, P. I. S. 1977. Aspectos biológicos das Orchidaceae de uma campina da Amazônia central. Acta Amazonica 2 (suppl.). Catling, P. M. and V. R. Catling. 1991. Anther cap retention in Tipularia discolor. Lindleyana 6: 113-116. Chase, M. W. 1985. Pollination of Pleurothallis endotrachys. Amer. Orch. Soe. Buli. 54: 431-434.

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